Editing Animal echolocation (section)

==== Whale evolution ====

[[Cetacea]]n evolution consisted of three main [[Evolutionary radiation|radiations]]. Throughout the middle and late [[Eocene]] periods (49-31.5 million years ago), [[archaeocete]]s, primitive toothed Cetacea that arose from terrestrial mammals, were the only cetaceans.<ref name="Gatesy Geisler Chang 2012">{{cite journal |last1=Gatesy |first1=John |last2=Geisler |first2=Jonathan H. |last3=Chang |first3=Joseph |author4=Buell, Carl |author5=Berta, Annalisa |author6=Meredith, Robert W. |author7=Springer, Mark S. |author8=McGowen, Michael R. |display-authors=3 |year=2012 |title=A phylogenetic blueprint for a modern whale |journal=[[Molecular Phylogenetics and Evolution]] |volume=66 |issue=2 |pages=479–506 |doi=10.1016/j.ympev.2012.10.012 |pmid=23103570}}</ref><ref name="Fordyce 1980">{{cite journal |last1=Fordyce |first1=R. E. |year=1980 |title=Whale evolution and oligocene southern-ocean environments | journal= Palaeogeography, Palaeoclimatology, Palaeoecology |volume=31 |pages=319–336 |doi=10.1016/0031-0182(80)90024-3 |bibcode=1980PPP....31..319F |doi-access=free }}</ref> They did not echolocate, but had slightly adapted underwater hearing.<ref name="Fordyce 2003">{{cite book |last=Fordyce |first=R. E. |year=2003 |chapter=Cetacean Evolution and Eocene-Oligocene oceans revisited |editor1=Prothero, Donald R. |editor2=Ivany, Linda C. |editor3=Nesbitt, Elizabeth A. |title=From Greenhouse to Icehouse: the Marine Eocene-Oligocene Transition |publisher=[[Columbia University Press]] |pages=154–170 |isbn=978-0-2311-2716-5}}</ref> By the late middle Eocene, acoustically isolated ear bones had evolved to give [[Basilosauridae|basilosaurid]] archaeocetes directional underwater hearing at low to mid frequencies.<ref name="Lindberg 2007">{{cite journal |last1=Lindberg |first1=D. R. |last2=Pyenson |first2=Nicholas D. |author2-link=Nicholas Pyenson |year=2007 |title=Things that go bump in the night: evolutionary interactions between cephalopods and cetaceans in the tertiary |journal=Lethaia |volume=40 |issue=4 | pages=335–343 |doi=10.1111/j.1502-3931.2007.00032.x|bibcode=2007Letha..40..335L }}</ref> With the extinction of archaeocetes at the onset of the [[Oligocene]] (33.9–23 million years ago), two new lineages evolved in a second radiation. Early mysticetes (baleen whales) and odontocetes appeared in the middle Oligocene in New Zealand.<ref name="Fordyce 1980"/> Extant odontocetes are [[monophyletic]] (a single evolutionary group), but echolocation evolved twice, convergently: once in ''[[Xenorophus]]'', an Oligocene [[Stem-group|stem]] odontocete, and once in the [[crown group|crown]] odontocetes.<ref name="Racicot 2019">{{cite journal |last1=Racicot |first1=Rachel A. |last2=Boessenecker |first2=Robert W. |last3=Darroch |first3=Simon A. F. |last4=Geisler |first4=Jonathan H. |year=2019 |title=Evidence for convergent evolution of ultrasonic hearing in toothed whales |journal=Biology Letters |volume=15 |issue=5 |pages=20190083 |doi=10.1098/rsbl.2019.0083 |pmid=31088283 |s2cid=155091623 |pmc=6548736 }}</ref> 

{{clade
|label1=<!--<ref name="Gatesy Geisler Chang 2012"/>--> 
|1={{clade
   |label1=[[Cetacea]]
   |1={{clade
      |label2='''''directional u/water hearing'''''
      |sublabel2=''mid/late [[Eocene]]''
      |2=[[Basilosauridae]] † 
      |1={{clade
         |label1=[[Odontoceti]] 
         |sublabel1=''[[Oligocene]]''
         |1={{clade
            |label1='''''echolocation'''''
            |sublabel1=''late [[Oligocene]]''
            |1=''[[Xenorophus]]'' † 
            |label2='''''echolocation'''''
            |2={{clade
               |1=[[Physeteroidea]]
               |2={{clade
                  |1=[[Ziphiidae]], etc.
                  |label2=''adaptive radiation''
                  |sublabel2=''[[Miocene]]''
                  |2=[[Delphinoidea]]
                  }}
               }}
            }}
         |label2='''''echolocation'''''
         |sublabel2=''middle [[Oligocene]]''
         |2=[[Mysticeti]]
         }} 
      }} 
   }}
}}

{| style="font-size: 10px; background: whitesmoke; float:right;"
|+ style="font-size:12px;" | '''Cetacean evolution timeline'''<ref name="Fordyce 1980"/>
|- style="background:lightgray;"
! scope="col" style="width: 50px;" | Epoch
! scope="col" style="width: 55px;" | Start date
! scope="col" style="width: 100px;" | Event
|- 
| [[Miocene]] || 23 [[Myr|mya]] || [[Adaptive radiation]], esp. of dolphins
|-
| [[Oligocene]] || 34 mya || [[Odontocetes]] echolocation
|-
| [[Eocene]] || 49 mya || [[Archaeoceti|Archaeocetes]] underwater hearing
|}

Physical restructuring of the oceans has played a role in the evolution of echolocation. Global cooling at the [[Eocene-Oligocene boundary]] caused a change from a [[Greenhouse and icehouse Earth|greenhouse to an icehouse world]]. Tectonic openings created the [[Southern Ocean]] with a free flowing [[Antarctic Circumpolar Current]].<!--<ref name="Fordyce 1980"/>--><ref name="Fordyce 2003"/><ref name="Lindberg 2007"/><ref name="Steeman_2009">{{cite journal |last1=Steeman |first1=Mette E. |last2=Hebsgaard |first2=Martin B. |last3=Fordyce |first3=R. Ewan |last4=Ho |first4=Simon Y. W. |last5=Rabosky |first5=Daniel L. |last6=Nielsen |first6=Rasmus |last7=Rahbek |first7=Carsten |last8=Glenner |first8=Henrik |last9=Sørensen |first9=Martin V. |last10=Willerslev |first10=Eske |display-authors=3 |title=Radiation of extant cetaceans driven by restructuring of the oceans |journal=Systematic Biology |volume=58 |issue=6 |pages=573–585 |date=December 2009 |pmid=20525610 |pmc=2777972 |doi=10.1093/sysbio/syp060 }}</ref> These events encouraged selection for the ability to locate and capture prey in turbid river waters, which enabled the odontocetes to invade and feed at depths below the [[photic zone]]. In particular, echolocation below the photic zone could have been a predation adaptation to [[Diel vertical migration|diel migrating]] [[cephalopods]].<ref name="Lindberg 2007"/><ref>{{cite journal |last1=Fordyce |first1=R. Ewan |last2=Barnes |first2=Lawrence G. |year=1994 |title=The evolutionary history of whales and dolphins | journal=Annual Review of Earth and Planetary Sciences |volume=22 |issue=1 | pages=419–455 |doi=10.1146/annurev.ea.22.050194.002223 | bibcode=1994AREPS..22..419F }}</ref> The family [[Delphinidae]] (dolphins) diversified in the [[Neogene]] (23–2.6 million years ago), evolving extremely specialized echolocation.<ref>{{cite journal | last1=McGowen |first1=Michael R. |last2=Spaulding |first2=Michelle |last3=Gatesy |first3=John |title=Divergence date estimation and a comprehensive molecular tree of extant cetaceans |journal=Molecular Phylogenetics and Evolution |volume=53 |issue=3 |pages=891–906 |date=December 2009 |pmid=19699809 |doi=10.1016/j.ympev.2009.08.018 }}</ref><ref name="Fordyce 2003"/>

Four proteins play a major role in toothed whale echolocation. [[Prestin]], a motor protein of the outer hair cells of the inner ear of the mammalian [[cochlea]], is associated with hearing sensitivity.<ref name="Liu Rossiter Xiuqun 2010">{{cite journal | last1=Liu |first1=Yang |last2=Rossiter |first2=Stephen J. |last3=Han |first3=Xiuqun |last4=Cotton |first4=James A. |last5=Zhang |first5=Shuyi |title=Cetaceans on a molecular fast track to ultrasonic hearing |journal=Current Biology |volume=20 |issue=20 |pages=1834–1839 |date=October 2010 |pmid=20933423 |doi=10.1016/j.cub.2010.09.008 |doi-access=free |bibcode=2010CBio...20.1834L }}</ref> It has undergone two clear episodes of accelerated evolution in cetaceans.<ref name="Liu Rossiter Xiuqun 2010"/> The first is connected to odontocete divergence, when echolocation first developed, and the second with the increase in echolocation frequency among dolphins. [[TMC1|Tmc1]] and Pjvk are proteins related to hearing sensitivity: Tmc1 is associated with hair cell development and high-frequency hearing, and Pjvk  with hair cell function.<ref name="Davies Cotton Kirwan 2012">{{Cite journal |last1=Davies |first1=K. T. J. |last2=Cotton |first2=J. A. |last3=Kirwan |first3=J. D. |last4=Teeling |first4=E. C. |last5=Rossiter |first5=S. J. |date=May 2012 |title=Parallel signatures of sequence evolution among hearing genes in echolocating mammals: an emerging model of genetic convergence |journal=Heredity |volume=108 |issue=5 |pages=480–489 |doi=10.1038/hdy.2011.119 |issn=1365-2540 |pmc=3330687 |pmid=22167055}}</ref> [[Molecular evolution]] of Tmc1 and Pjvk indicates positive selection for echolocation in odontocetes.<ref name="Davies Cotton Kirwan 2012"/> [[CLDN14|Cldn14]], a member of the tight junction proteins which form barriers between inner ear cells, shows the same evolutionary pattern as Prestin.<ref>{{cite journal | last1=Xu |first1=Huihui |last2=Liu |first2=Yang |last3=He |first3=Guimei |last4=Rossiter |first4=Stephen J. |last5=Zhang |first5=Shuyi |title=Adaptive evolution of tight junction protein claudin-14 in echolocating whales |journal=Gene |volume=530 |issue=2 |pages=208–214 |date=November 2013 |pmid=23965379 |doi=10.1016/j.gene.2013.08.034 }}</ref> The two events of protein evolution, for Prestin and Cldn14, occurred at the same times as the tectonic opening of the [[Drake Passage]] (34–31 Ma) and Antarctic ice growth at the Middle [[Miocene]] climate transition (14 Ma), with the divergence of odontocetes and mysticetes occurring with the former, and the speciation of Delphinidae with the latter.<ref name="Steeman_2009"/>

The evolution of two cranial structures may be linked to echolocation. Cranial telescoping (overlap between [[Frontal bone|frontal]] and [[maxilla]]ry bones, and rearwards displacement of the nostrils<ref name="Roston Roth 2019">{{cite journal | last1=Roston | first1=Rachel A. | last2=Roth | first2=V. Louise | title=Cetacean Skull Telescoping Brings Evolution of Cranial Sutures into Focus | journal=The Anatomical Record | publisher=Wiley | volume=302 | issue=7 | date=8 March 2019 | issn=1932-8486 | doi=10.1002/ar.24079 | pages=1055–1073| pmid=30737886 | pmc=9324554 }}</ref>) developed first in [[Xenorophidae|xenorophids]]. It evolved further in stem odontocetes, arriving at full cranial telescoping in the crown odontocetes.<ref name="Churchill Geisler Beatty 2018">{{Cite journal |last1=Churchill |first1=Morgan |last2=Geisler |first2=Jonathan H. |last3=Beatty |first3=Brian L. |last4=Goswami |first4=Anjali |date=2018 |title=Evolution of cranial telescoping in echolocating whales (Cetacea: Odontoceti) |url=https://onlinelibrary.wiley.com/doi/abs/10.1111/evo.13480 |journal=Evolution |volume=72 |issue=5 |pages=1092–1108 |doi=10.1111/evo.13480 |pmid=29624668 |s2cid=4656605 |issn=1558-5646|url-access=subscription }}</ref> Movement of the nostrils may have allowed for a larger nasal apparatus and [[Melon (cetacean)|melon]] for echolocation.<ref name="Churchill Geisler Beatty 2018"/> This change occurred after the divergence of the neocetes from the basilosaurids.<ref name="Coombs Clavel Park 2020">{{Cite journal |last1=Coombs |first1=Ellen J. |last2=Clavel |first2=Julien |last3=Park |first3=Travis |last4=Churchill |first4=Morgan |last5=Goswami |first5=Anjali |date=2020-07-10 |title=Wonky whales: the evolution of cranial asymmetry in cetaceans |journal=BMC Biology |volume=18 |issue=1 |page=86 |doi=10.1186/s12915-020-00805-4 |issn=1741-7007 |pmc=7350770 |pmid=32646447 |doi-access=free }}</ref> The first shift towards cranial asymmetry occurred in the Early Oligocene, prior to the xenorophids.<ref name="Coombs Clavel Park 2020"/> A xenorophid fossil (''Cotylocara macei'') has cranial asymmetry, and shows other indicators of echolocation.<ref name="Geisler Colbert Carew 2014">{{Cite journal |last1=Geisler |first1=Jonathan H. |last2=Colbert |first2=Matthew W. |last3=Carew |first3=James L. |date=April 2014 |title=A new fossil species supports an early origin for toothed whale echolocation |url=https://www.nature.com/articles/nature13086 |journal=Nature |volume=508 |issue=7496 |pages=383–386 |doi=10.1038/nature13086 |pmid=24670659 |bibcode=2014Natur.508..383G |s2cid=4457391 |issn=1476-4687|url-access=subscription }}</ref> However, basal xenorophids lack cranial asymmetry, indicating that this likely evolved twice.<ref name="Coombs Clavel Park 2020"/> Extant odontocetes have asymmetric nasofacial regions; generally, the [[median plane]] is shifted to the left and structures on the right are larger.<ref name="Geisler Colbert Carew 2014"/> Both cranial telescoping and asymmetry likely relate to sound production for echolocation.<ref name="Churchill Geisler Beatty 2018"/>