Animal domestication

and behaviour

With focus on the domestication of

the dog (Canis familiaris)

DOKTORANDUPPSTATS

Christina Hansen, PhD student

Stockholm University

 

 

 

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TABLE  OF  CONTENTS  

 

Part  I  

1. Abstract             3  

2. Introduction  to  domestication           4  

3. Selection  for  tameness  –  the  farm  fox  experiment       6  

4. Cause  and  effect  of  domestication           11  

1. Neuro-­‐endocrine  causation  of  the  domesticated  phenotype     13  

1. Thyorid  horomone  metabolism         14  

2. Glucocorticoids           15  

 

Part  II  

5. Domestication  of  the  dog           18  

1. The  ancestral  origin  of  the  domestic  dog         18  

2. When  was  the  dog  domesticated?         19  

3. The  geographical  origin  of  the  domestic  dog       20  

4. How  was  the  dog  domesticated?         22  

6. Conclusion             27  

7. References             28  

 

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1. ABSTRACT  

Part  I  of  the  paper  is  an  overview  of  the  domestication  process.  Man  started  domesticating  livestock  

animals   around   the   time   when   the   society   structure   gradually   changed   from   hunter-­‐gatherers   to  

agriculture   about   10,000   years   ago.   Domestication   is   an   evolutionary   process   driven   by   natural,  

conscious   and   un-­‐conscious   selection   in   which   a   population   of   animals   gradually   adapts   to   life   in  

captivity.   Some   animals   are   naturally   more   equipped   for   a   live   as   domesticated   animals,   and   the  

domesticated  species  are  largely  biased  towards  ungulates  and  birds.  Domestication  is  strongly  driven  

by  selection  for  desirable  behavioural  traits  such  as  tameness  and  decreased  aggression.  A  long-­‐term  

study   beginning   in   the   Soviet   Union   in   the   late   1950’s   showed   how   quickly   some   degree   of  

domestication  could  be  obtained  by  selectively  breeding  for  tameness  in  a  population  of  farm  foxes.  

With  the  behavioural  changes  brought  about  in  the  study  dramatic  morphological  changes  followed  as  

well;   changes   that   are   characteristic   across   various   domesticated   species.   These   changes   are   as   a  

syndrome  referred  to  the  domesticated  phenotype.  The  underlying  mechanisms  for  these  changes  are  

found  in  alterations  of  the  physiology,  especially  in  the  neuro-­‐endocrine  system.  

 

Part   II   of   the   paper   evolves   around   the   domestication   of   the   dog.   The   domestication   of   the   dog  

remains  a  popular  and  quite  controversial  subject.  The  dog  was  domesticated  from  the  grey  wolf  at  

least  15,000  years  ago,  but  both  fossil  findings  and  molecular  analyses  points  in  the  direction  that  the  

dog  is  in  fact  much  older  than  that.    Using  arguments  based  on  genetic  analyses  there  is  an  on-­‐going  

discussion   if   the  domestic   dog  originated   from  Southern   East  Asia   or   from  Europe/the  Middle   East.  

The   question   remains   unanswered.   As   do   the   question   of   how   the   dog   was   domesticated.   The  

individual-­‐based  selection  theory  suggests  that  the  domestication  of  the  dog  started  with  taming  and  

breeding   of   individual   wolves,   whereas   the   population-­‐based   selection   theory   suggests   that   the  

wolves   them-­‐selves   started   the   domestication   process   by   gradually   increasing   the   acceptance   of  

humans.    With   little   conclusive   evidence   on   the   subject   as   a  whole,   this   part   of   the   paper   gives   an  

overview  of  the  different  perspectives  of  the  domestication  of  the  dog.  

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2. INTRODUCTION  TO  DOMESTICATION  

It   has   proven   problematic   to   obtain   general   consensus   about   the   definition   of   domestication  

(Crockford,   2002;   Gentry   et   al.,   2004;   Driscoll   et   al.,   2009;   Morey,   2010;   Zeder,   2012).   A   probable  

explanation  for  this  discrepancy  is  the  difficulties  in  understanding  the  various  intermediate  stages  in  

the  continuum  framed  by   the  two  extremes  observable   for  us   today;   the  wild  ancestor  and   its   truly  

domesticated  derivative.  Domestication  is  not  necessarily  the  only  alternative  to  a  wild  existence,  and  

the  concept  could  be  looked  upon  as  a  gradual  process  with  little  or  no  absolute  values  when  we  try  

to  quantify   the  degree  of  domestication   in  an  animal  originated   from  a  wild  ancestor   (Gentry  et  al.,  

2004;  Dobney  &  Larson,  2006;  Driscoll  et  al.,  2009).  However,  domestication  in  a  broader  perspective  

can  be  described  as  an  on-­‐going  evolutionary  process  that  happens  through  a  combination  of  genetic  

and   environmental   induced   developmental   changes   occurring   over   generations   through   natural,  

conscious   and   unconscious   selection.     By   this   process   a   population   of   animals   gradually   becomes  

adapted  to  man  and  to  the  captive  environment  he  provides(Price,  2002;  Gentry  et  al.,  2004;  Morey,  

2010;  Zeder,  2012).  

 

Gentry   et   al.   (2004)   states   four  main   characteristics   that   collectively   describes   the  most   developed  

form   of   a   domesticated   animal:     1)   Breeding   should   be   under   human   control,   2)   the   domesticated  

animal  should  be  of  use  to  humans  by  providing  some  sort  of  product  or  service,  3)  the  animal  should  

display  a  behaviour  that  can  be  classified  as  “tame”,  and  4)  the  animal  has  been  selected  away  from  its  

original  wild  type.  Isaac  (via  Crockford,  2002)  stated  a  very  similar  description  of  a  truly  domesticated  

animal   already   back   in   1970,   and   adds   a   fifth   point   to   the   above;   that   the   animal’s   survival   should  

depend  on  humans,  whether  voluntarily  or  not.  However,   far   from  all  domesticated  animals  actually  

possess   all   these   features,   and   we   might   find   ourselves   struggling   with   placing   particular   animals  

and/or  species  in  strictly  wild  or  strictly  domesticated  categories  (Gentry  et  al.,  2004).    

 

Part  I  

  5  

Animals   possessing   certain   behavioural   and   physical   traits   are   considered   more   suited   for  

domestication   than   others,   and   can   be   described   as   being   “pre-­‐adapted”   to   become   domesticated  

(Price,  2002;  Drsicoll  et  al.,  2009;  Zeder,  2012.  The  level  of  pre-­‐adaptation  is  determined  by  the  capacity  

of   individual  animals  of  a  given  species  to  adapt  to  a  captive  environment.  Thus  parameters  such  as  

social   organization,   reproductive   behaviour,   dietary   needs,   habitat   requirements   and   response   to  

humans   are   all   factors   in   determining   a   species   potential   for   domestication   (Diamond,   2002;   Price,  

2002;   Driscoll   et   al.,   2009;   Zeder,   2012).   Species   displaying   a   natural   behaviour   resembling   the  

behaviour   expected   and   possible   in   captivity   is   considered   to   posses   the   largest   degree   of   pre-­‐

adaptation.    Pre-­‐adaptational  traits   in  the  natural  range  of  a  species’  ecology  are  primarily  traits  that  

make   it  easier   for  humans  to   in-­‐cooperate   themselves   in   the   life  of   the  animals  by   taking   leadership  

and   controlling   and  manipulating   reproductive   behaviour   and   food   sources   (Diamond,   2002;   Zeder,  

2012).   Thus   species   with   large   gregarious   and   social   group   structure   are   more   pre-­‐adapted   than  

territorial   species   living   in   family   groups,   and   species  with   promiscuous   and/or   polygamous  mating  

systems  are  more  pre-­‐adapted  than  species  with  a  monogamous  mating  system.  Furthermore,  species  

with  a  more  flexible  ecology,  such  as  a  generalist  and  omnivores  are  more  flexible  in  their  adaptation  

to   captivity   than   species   with   highly   specialized   dietary   preferences   (Price,   2002;   Zeder,   2012).   The  

majority  of  domesticated  species  are  to  a  large  (Cameron-­‐Beaumont  et  al.,  2002;  Diamond,  2002;  Price,  

2002;   Driscoll   et   al.,   2009)   extent   biased   towards   ungulates   and   gallinaceous   birds,   which   strongly  

indicates  that  pre-­‐adaptation  for  domestication  was  present   in  the  wild  phenotype  of  these  species.  

This  suggests  that  pre-­‐adaptation  varies  with  species’  and  that  different  orders  of  animals  might  not  

possess  the  same  capacity  for  domestication  (Diamond,  2002;  Price,  2002;  Cameron-­‐Beaumont  et  al.,  

2002;  Jensen,  2005;  Driscoll  et  al.,  2009).  

When   agriculture   (and   thereby   the   domestication   of   plants)   emerged   about   10,000   years   ago  

(Diamond,  2002;  Price,  2002),  it  is  believed  that  the  initial  domestication  of  the  larger  ungulate  species,  

including   cattle,   directly   followed   this   process   (Diamond,   2002;   Price,   2002).   Pigs   (Sus   scrofa)   are  

believed   to   have   been   domesticated   9,000   years   ago   (Jansen   et   al.,   2002;   Price,   2002),   and   rabbits  

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(Oryctolagus   cuniculus)     2,500   years   ago   (Price,   2002).     When   horses   (Equus   caballus)   were  

domesticated   remains   somewhat   inconclusive;   authors   speculate   in   a   timespan   from   almost   12,000  

years   ago   (Bruford  et   al.,   2003)   to  6,000  years   ago   (Vila,   2001;  Price,   2002).   The  discrepancy  on   the  

subject   has   lead   to   the   proposal   that   horses   were   domesticated   numerous   times   with   various  

geographical  origins  (Bruford  et  al.,  2003).  

 

Tameness  can  be  defined  as  a  behavioural  phenotype  in  which  an  individual  displays  some  degree  of  

decreased  aggression  towards,  and  increased  acceptance  of,  humans.  Individuals  displaying  tameness  

are   also   likely   to   show   of  motivation   to   approach   and/or   initiate   contact   with   humans   (Trut,   2001;  

Price,  2002;  Albert  et  al.,  2008).  Some  wild  animals  can  display  various  degrees  of  tameness  and  vice  

versa  some  domestic  animals  may  display  decreased  tameness  (Diamond,  2002;  Driscoll  et  al.,  2009).  

Tameness  should  be  separated   from  tameability;   the  capacity   for  an  animal  or   species   to  be   tamed.  

Tameability   is  believed  to  be  a  heritable  trait  and  could  thereby  be  a  part  of   the  genetic  heritage  of  

domestication.  Hence,  some  species  and   individuals  are  expected  to  be  more  tameable  than  others,  

which   is   in   accordance  with   the  pre-­‐adaptational   theory   (Diamond,   2002;   Price,   2002;  Driscoll   et   al.,  

2009).  Taming  on  the  other  hand,   is  a   learning  process   in  which  an   individual  throughout   its   lifespan  

reduces   its   avoidance  behaviour   and  aggression  directed  at  humans  and   increases   its  willingness   to  

approach   humans   (Price,   2002).   Domestication   and   taming   are   two   very   different   concepts   and  

processes,  and  one  does  not  necessarily  result  in  the  other  (Diamond,  2002;  Price,  2002).  Taming  of  an  

individual   is  brought  about  by  a  conditioned  behavioural  modification   (Belyaev  et  al.,   1985;  Spady  &  

Ostrander,   2007;   Trut,   1999),  whereas   domestication   is   a   heritable   permanent   genetic   alteration   of  

species  and/or  breeds  (Price,  2002).    

 

3. SELECTION  FOR  TAMENESS  -­‐  THE  FARM-­‐FOX  EXPERIMENT  

In  1959  the  Russian  geneticist  Dimitri  K.  Belyaev  (1917-­‐1985)  initiated  a  long-­‐term  study  to  investigate  

the  genetics  behind  the  evolutionary  process  of  domestication  (Belyaev  et  al.,  1985;  Trut,  1999;  Spady  

  7  

and  Ostrander,  2007).  The  study  was  based  on  the  hypothesis  that  the  striking  similarity  we  see  across  

a   broad   spectrum   of   domesticated   species   today,   is   brought   about   as   by-­‐products   of   selection   for  

behaviour   (Trut,   1999;   Trut   et   al.,   2004;2009;   Morey,   2010).   Belyaev   believed,   that   the   methodical  

selection  for  behavioural  traits  alone  could  explain  the  general  domesticated  phenotype,  and  he  was  

especially   interested   in   the   process   in   which   dogs   were   domesticated   from   wolf   ancestors   (Trut,  

1999).  Thus,  he  began  his  study  at  The  Institute  of  Cytology  and  Genetics   in  Novosirbirsk,  Siberia  –  a  

study  that  should  become  quite  remarkable  and  important  in  our  understanding  of  the  domestication  

process  (Trut  et  al.,  2009;  Morey,  2010).  

 

The   study   species   was   silver   foxes   (Vulpes   vulpes),   bred   as   farmed   foxes   for   their   fur.   The   main  

hypothesis  of  the  study  was  based  on  Belyaev’s  own  observations  that  while  the  foxes  were  generally  

strongly  aggressive  and  fearful  towards  their  human  caretakers  and  handlers,  a  small  fraction  of  them  

displayed   a   decreased   level   of   aggression   and   fear   (Morey,   2010).   This   led   Belyaev   to   suggest   that  

behavioural   variation   could   be   the   primarily   causation   and   driving   force   of   variation   among  

domesticates  in  general  (Trut  et  al.,  2009).  To  investigate  whether  his  theories  were  accurate,  Balyaev  

created  a  strain  of  foxes  selectively  bred  strictly  and  solely  on  the  trait  tameness  and  compared  them  

to  an  unselected  strain.  The  founder  population  of  the  tame  fox  strain  consisted  of  100  females  and  30  

males   carefully   selected   from   various   fur-­‐farm  populations   (Trut,   1999;   Trut   et   al.,   2004;   Spady   and  

Ostrander,  2007).  The  foxes  were  chosen  based  only  on  observational  evaluations  of  their  degree  of  

tameness,   as   an  experimenter   approached  and  opened   their   cage.  Where  wild-­‐type   foxes  displayed  

aggressive  and/or  avoidance  behaviour  towards  humans,  about  10%  of  the  farm-­‐fox  population  (more  

females  than  males)  reviewed  for  selection  displayed  a   lowered,  or   in  some  cases  non-­‐present,  wild-­‐

type   response   (Fig.   1)   -­‐   those  were   the   foxes   chosen   for   the   founder   population   (Trut   et   al.,   2009;  

Morey,  2010).    

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For   every   generation   following   these   founder   foxes,   only   the   tamest   individuals   were   allowed   to  

breed.  Pups  were  raised  with  their  mothers  until  approximately  two  months  of  age  and  then  moved  to  

a   different   cage  with   their   littermates.   Here   the   pups  would   stay,   until   they  where   put   in   separate  

cages  at  three  months  of  age  (Trut  et  al.,  2004).  To  assess  the  level  of  tameness  in  individual  foxes,  the  

behavioural   testing  began  already  when  pups  were  one  month  old;  here   they  were  offered   food  by  

hand-­‐feeding  while  the  experimenter  attempted  to  stroke  them.  Each  pup  was  submitted  to  this  test  

twice;  once  in  a  social  context  when  in  an  enclosure  with  littermates  and  once  in  a  solitary  context  in  a  

cage.   This   test  was   repeated  once   a  month   until   the   pups  were   six   or   seven  months   old.   Reaching  

sexual  maturation  at  approximately  six  to  eight  months  of  age,  the  foxes  were  categorized  according  

to  three  classes  based  on  the  degree  of  tameness  (Trut,  1999;  Spady  and  Ostrander,  2007):  

 

Class  III:     Foxes   in   this   class   displayed   the   least   tame   behaviour;   they   displayed   both   fearful   and  

aggressive   behaviour,   by   attempting   to   flee   from   or   bite   the   handler   when   stroked   or  

handled.  However,   by   accepting  hand-­‐feeding   these   foxes  were   still   considered   tamer   than  

the  most  docile  farm-­‐bred  foxes.  

 

Class  II:   Foxes   in   this   class   accepted   to   be   handled   and   stroked   without   displaying   aggressive   or  

fearful  behaviour,  but  they  did  not  show  initiative  to  approach  the  handler  and  they  showed  

no  friendly  disposition  towards  the  handler.  

 

Fig.  1.  On  the  left,  a  fox  displaying  the  wild  phenotype,  being  stressed,  scared  and  aggressive  when  humans  approach   the   cage.   On   the   right,   displaying   an   altered   phenotype,   being   curious   and   friendly   to   human  contact.  From  Trut  et  al.,  2009.  

 

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Class  I:     Foxes   in   this   class   showed  clear   friendliness   towards   the  handler  by  wagging   their   tails  and  

whining  when  approached.  They  readily  accepted  hand-­‐feeding,  stroking  and  handling.  

 

Class  IE:   This  class  was  not  part  of  the  original  set-­‐up,  but  was  added  in  the  sixth  generation  of  strict  

selective  breeding  for  tameness  as  a  domesticated-­‐elite  class.  Those  foxes  actively  sought  the  

attention  from  handlers  even  when  not  approached,  and  would  whimper  and  wag  their  tails  

to  induce  human  contact.  They  would  lick  and  sniff  experimenters  once  contact  was  initiated.  

 

 

The  amount  of  foxes  qualifying  for  breeding  in  each  generation  were  under  strict  control,  and  only  3%  

of   the  males  and  8-­‐10%  of   the   females   in   the  highest   tameness-­‐classes  were  used  as  parents   for   the  

next   generation,   creating   an   extreme   selection   pressure   for   tameness   (Trut   et   al.,   2004;   2009).  

Generation   six   was   the   first   generation   containing   elite   individuals   (EI);   out   of   213   offspring   going  

through  the  behavioural  test  procedure  only  4  individuals  were  classified  as  belonging  to  class  EI.  This  

translates  to  1.8%  of  the  tested  population.  In  the  10th  generation  66  out  of  370  individuals  tested  were  

elite  animals,   increasing  the  elite  percentage  to  17.8%.   In  generation  20,  1438   individuals  qualified  for  

behavioural   testing,   of   those   503,   or   35%,  were   elite   animals.   In   the   30th   generation   1641   individuals  

were  tested,  of  those  804  or  49%  were  elite  animals.  The  elite  percentage  reached  71.2%  in  generation  

42,  where  642  out  of  902   individuals  tested  were  elite  animals  (Mignon-­‐Grasteau  et  al.,  2005;  Trut  et  

al.,  2009).  The  changes  in  tameness  over  generations  are  illustrated  in  table  1.  

 

Table   1   (from  Trut  et   al.,   2004):   The  proportion  of   individuals  belonging   to  Class   IE   in  different  generations  

during  selective  breeding  for  tameness.  

Year   Generation  No.  of  offspring  

tested  

No.  of  elite  

individuals  Elite  percentage  

1965   F6   213   4   1.8  

1970   F10   370   66   17.8  

1980   F20   1438   503   35.0  

1990   F30   1641   804   49.0  

2002   F42   902   642   71.2  

 

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Impressive   as   these   results   are,   tame   foxes   with   wagging   tails   and   a   dog-­‐like   friendliness   towards  

humans   were   not   the   only   outcome   of   the   farm-­‐fox   experiment.   Jensen   (2002)   describes   various  

general   traits   characteristic   for   the  “domesticated  phenotype”,  which  apart   from  generally   reduced  

body   size   and   altered   reproductive   behaviour,   includes   additional   morphological   and   physiological  

alterations.  A  very  characteristic  external  morphological  feature  seen  in  the  domesticated  phenotype  

is  the  alteration  of  coat  and  plumage  colours.  Depigmentation  resulting  in  varying  shapes  and  degrees  

of   white   patchy   colouration   is   thus   seen   in   a   wide   range   of   domesticated   animals,   such   as   rabbits  

(Oryctolagus  cunticulus),  pigs   (Sus  scrofa  domesticus),  cows  (Bos  taurus),  horses   (Equus  caballus)  and  

dogs   (Canis   familiaris)   (Jensen,   2002;   Trut   et   al.   2009).   This   typical   white   colour   pattern   seen   in  

domesticates   might   be   explained   by   relaxed   selection   pressures   on   predator-­‐avoidance   (Mignon-­‐

Grasteau   et   al.,   2005).   Other   external   morphological   traits   that   are   repeated   across   domesticated  

species  are  features  such  as  curly  tails  and  floppy  ears  (Trut  et  al.,  2009).  The  general  occurrence  of  

phenotypically  similarities  across  a  wide  range  of  species  seems  unlikely  to  have  its  origin  in  separate  

mutations  of  structural  homologous  genes,  but  rather  to  be  a  result  of  the  altered  selection  pressures  

brought   about  by  domestication.  Darwin   speculated   about   this   very  hypothesis   in  Origin  of   Species  

(1859),   and   many   after   him   did   as   well   –   including   Belyaev   (Trut,   1999;   Trut   et   al.,   2004;   Spady   &  

Ostrander,  2007;  Trut  et  al.,  2009;  Morey,  2010).    

 

As   it   turned  out,   it  would   seem   that  Belyaev  had  been  astonishingly   correct   in  his   initial   hypothesis  

(Spady   and   Ostrander,   2007),   that   the   morphological   similarities   seen   across   a   wide   range   of  

domesticated   species   could   be   explained   as   by-­‐products,   or   correlated   traits,   for   selection   on  

tameness   alone.   Thus,   Belyaev   and   his   team   did   not   only   see   behavioural   alterations   in   the   study  

population,  they  also  saw  striking  changes  in  morphology,  all  of  which  were  very  much  in  accordance  

with   the   domesticated   phenotype   as   described   above.   After   only   8   to   10   generations   colour  

alterations  started   to  appear   in   the  study  population   (Trut,   1998;   1999;  Trut  et  al.,   2004).  Molting   in  

brown   and   yellow   colours   started   deviating   from   the   standard   silver   grey   coat   of   the   foxes   and  

  11  

characteristic   localized   depigmentation,   often   located   on   the   face   in   shape   of   a   star   (piebaldness)  

started  to  occur.  Piebaldness  is  widely  spread  in  domestic  animals,  and  is  claimed  to  be  one  of  the  first  

changes  appearing  in  domesticated  populations  across  species  (Trut,  1998;  1999).  As  an  example,  pale  

and   spotted   coat   colourings   have   been   reported   to   occur   in   the   very   early   stages   of   dog  

domestication  at  least  3,000  years  BC  (Hemmer,  1990;  Trut  et  al.,  2004).  After  a  few  more  generations  

of  selection  for  tameness,   floppy  ears  and  curly  tails  starting  to  appear   in  the  study  population,  and  

after   15   to   20   generations   some   of   the   foxes   would   display   shortened   tails,   shortened   legs   and  

attenuated  skull  morphology,  such  as  widened  skulls,  shorter  snouts  and  disproportionate   jaws  (Fig.  

2)  (Trut,  1999).                                  

 

         

4. CAUSE  AND  EFFECT  OF  DOMESTICATION  

Domestication   is   to   a   large   extent   driven   by   conscious   selection   for   desirable   traits,   which   in   turn  

might  lead  to  unconscious  selection  for  correlated  traits,  as  elegantly  illustrated  in  the  farm-­‐fox  study;  

thus  the  domesticated  phenotype  likely  contains  various  traits  that  were  not  intended,  at  least  not  to  

begin  with   (Trut,   1999;   Trut   et   al.,   2004;   Spady   &   Ostrander,   2007;   Trut   et   al.,   2009;  Morey,   2010).  

Fig.   2.     A   few  examples  of   the   morphological  changes   that   followed  the   selection   only   for  tameness   in   the   farm  fox   project.   Top   left:  two   fox   kits   of   which  one   has   visible   floppy  ears.   Top   right:   a   fox  with  a   remarkable  short  tail.   Middle   right:   a   fox  with   curly   tail.   Bottom  right:   fox   kits   with  distinct   and   dog-­‐like  white   pigmentation.  Bottom   middle:   a   fox    with   distinct   white  pigmentation   exhibiting  dog-­‐like   play   behaviour.  Bottom  left:  a  young  fox  displaying   an   extreme  degree   of   tameness  towards   its   handler  (Trut,  1999;  Byrne,  2005;  Trut  et  al.,  2009).  

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Genes   control   phenotypic   variance,   and   thus  when  we   select   for   traits,  we  are   selecting   for   certain  

genes  or  the  alteration  of  the  expression  of  certain  genes  (Jensen,  2006).      

 

Increased  brain  size  has  been  linked  with  refinement  of  sensory  organs,  motor  skills  and  behavioural  

flexibility  (Diamond,  2002;  Sol  et  al.,  2008),  and  it  seems  reasonable  to  assume  that  these  are  essential  

elements  for  wild  animals  to  survive.  Domesticates  in  fact  do  show  an  overall  decrease  in  relative  brain  

size   when   compared   to   their   similar   sized   wild   relatives:   pigs   (Sus   scrofa)   36%,   turkeys   (Meleagris  

gallopavo)  30%,  dogs  (Canis  familiaris)  29%,  sheep  (Ovis  aries)  24%,  horses  (Equus  caballus)  14%  and  rats  

(Rattus  norvegicus)  8%   (Kruska,   1988;  Clutton-­‐Brock,   1992;  Kruska,   1996;  Diamond,   2002;  Price,   2002;  

Jensen,  2002;  Zeder,  2012;).  The  brain  is  a  very  costly  organ  to  develop  and  maintain,  and  in  a  captive  

environment,   where   survival   is   no   longer   a   daily   struggle,   it   makes   good   sense   that   the   selective  

pressure   on   brain   size   eventually   became   relaxed   (Diamond,   2002;   Byrne   &   Corp,   2004;   Sol   et   al.,  

2008).  As  increased  relative  brain  size  has  been  linked  to  enhanced  cognitive  function  (Byrne  &  Corp,  

2004;  Sol  et  al.,  2005),  and  it  naturally  raises  the  question  if  domesticates  then  have  impaired  cognitive  

functionality   compared   to   their   wild   counterparts.   However,   a   smaller   relative   brain   size   is   not  

necessarily   the   same   as   a   lowered   level   of   cognition   (Cooper   et   al.,   2003).   Cognition   is   a   broad  

category   implicating   various   forms   of   behavioural   capacity,   and   for   instance   the   social   form   of  

cognition   has   been   shown   to   be   linked   the   complexity   and   size   of   a   specific   part   of   the   brain,   the  

neocortex,   and   not   the   total   size   of   the   brain   (Kruska,   1988;   Cooper   et   al.,   2003;   Sol   et   al.,   2005;  

Dunbar  &  Bever,  2010).    Furthermore,  it  has  been  suggested  that  domestic  animals  might  outperform  

their  wild  relatives   in   learning  tests;  while  wild  (but  tamed)   individuals  do  have   larger  relative  brains  

than  domesticated   conspecifics,   they  have  also  maintained  an  enhanced   sensory   system,  which  will  

make  them  more  perceptual  to  external  stimuli.  Therefore  wild  individuals  could  be  expected  to  have  

a  general  higher  baseline  level  of  vigilance,  which  might  divert  their  focus  from  the  learning  task  in  a  

test  situation  (Kruska,  1988).  

 

  13  

Many  authors  have  led  our  attention  to  the  phenomenon  “domesticated  phenotype”  (Clutton-­‐Brock,  

1992;  Trut,  1999;  1998;  Crockford,  2002;  Price,  2002;  Jensen,  2002;  Driscoll  et  al.,  2009).  Adding  to  these  

morphological  changes  described  in  the  farm-­‐fox  study,  a  general  reduction  in  body  size  is  seen  when  

comparing  domesticates  with  their  wild  relatives  (Tchernov  &  Horwitz,  1991;  Price,  2002;  Jensen,  2002;  

Jensen,   2006).   Shortening   and   altered   proportions   of   the   skull   and   legs   are   also   considered   to   be  

changes   related   to   domestication   (Clutton-­‐Brock,   1992;   Jensen,   2006).   Reproductive   biology  

represents   another   distinct   difference,   when   comparing   wild   living   ancestral   species   with   their  

domesticated   relatives;   in   general   we   see   earlier   sexual   maturation,   lowered   generation   time,  

increased   reproductive   rates   and   larger   litter   sizes   in   domesticated   animals   (Belyaev   et   al.,   1985;  

Tchernov  &  Horwitz,  1991;  Künzl  &  Sachser,  1999;  Price,  2002;  Jensen,  2006).    

 

It  might  seem  to  be  an  overwhelming  task  to  connect  all   these  alterations  and  preferences  through  

cause  and  effect,  but   it   remains  clear   that  behaviour  and  attenuation  capacity  of  behaviour   remains  

key   in   animal   domestication;  when  we   select   for   tameness   as   a   behavioural   trait,  we  unconsciously  

select  for  the  mechanisms  and  correlated  traits  associated  with  tameness  as  a  behavioural  trait.  Thus  

the  intense  artificial  selection  pressures  induced  upon  domesticated  animals  are  for  the  vast  majority  

primarily   driven   by   desirable   behavioural   attributes   (such   as   decreased   fear   of   humans,   lowered  

aggression,  trainability  etc.)  and  secondary  with  physiological  and  morphological  preferences    (Zeder,  

2012).  But  what  are  we  actually  selecting  upon  if  we  select  for  behavioural  traits  –  just  as  Belyaev  did  

on  the  farm-­‐foxes?  If  behaviour  is  the  effect,  then  what  is  the  cause?    

 

                   4.1    Neuro-­‐endocrine  causation  of  the  domesticated  phenotype  

One   of   the   most   fundamental   effects   of   domestication   is   the   alteration   of   the   neuro-­‐endocrine  

system,   in   turn   influencing   various   physical   and   behavioural   traits   in   domesticated   animals.   Thus  

domesticates   express   an   attenuated   hormonal   profile   due   to   alterations   of   activity   in   different  

secretion  systems  (Crockford,  2002;  Dobney  &  Larson,  2006).      

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                       4.1.1    Thyorid  hormone  metabolism  

The  morphological,  physiological  and  behavioural  changes  we  see  from  wild  type  to  domesticate  are  

for   the   vast   majority   traits   that   are   under   the   influence   of   thyroid   metabolism   (Crockford,   2002).  

Indications   have   been   found   that   several   traits   associated   with   domestication   to   a   great   extent  

resemble  symptoms  for  hypothyroidism.  Thyroid  hormone  metabolism  plays  a  crucial  role  in  physical  

and  cognitive  development,  both   in   the  embryonic  and  postnatal   state,  and  have  been  stated  to  be  

key  to  domestication  through  its  profound  effect  on  ontogeny  in  animals  (Crockford,  2002;  Dobney  &  

Larson,  2006).   In  a  comparative  study  on   lab  rats  and  wild  rats,   it  was  found  that  domesticated  rats  

had  significantly  smaller  thyroid  glands  compared  to  wild  rats.  Furthermore,  the  decreased  gland  size,  

and   thus   decreased   secretion   levels,   in   domesticated   rats   also   reduced   flight   behaviour   when  

compared  to  their  wild  counterparts  (Dobney  &  Larson,  2006).  Another  very  interesting  study  on  the  

effects  of  thyroid  hormones   in  rats  showed  how  thyroid  hormones  affect  growth  and  development;  

rat  embryos  were  manipulated  so  that  they  became  hypo-­‐thyroidic  while  still  in  the  womb  and  again  at  

the  age  of  18  days  after  birth,  and  compared  with  non-­‐manipulated  rats.  Hypo-­‐thyroidic  rats  displayed  

significant   morphological   differences   from   non-­‐mainpulated   rats,   including   smaller   overall   size,  

shorter   muzzle   and   floppy   ears   (Crockford,   2002).   Those   features   are   all   considered   to   be   traits  

included  in  the  “domesticated  phenotype”  as  described  above  (Jensen,  2002;  Trut  et  al.,  2009;  Hare  et  

al.,   2012),   and   these   traits   also   represents   the   phenomenon   of   paedomorphism   (Crockford,   2002;  

Dobney  &  Larson,  2006).  Paedomorphism  is  the  retention  of  juvenile  physiological,  morphological  and  

behavioural   characteristics   into   adult   life,   and   is   believed   to   represent   another   typical   sign   of  

domestication  (Clutton-­‐Brock,  1992;  Morey,  1994;  Goodwin  et  al.,  1997;  Crockford,  2002;  Cooper  et  al.,  

2003;  Driscoll  et  al.,  2009;  Hare  et  al.,  2012).  It  has  been  suggested  that  paedomorphism  might  be  the  

result   of   conscious   selection   for   docility,   which  would   equal   selection   of   animals   displaying   slower  

reaction   patterns   to   external   stimuli   and   thus   lowered   and   naive   perception   of   their   surroundings  

(Clutton-­‐Brock,  1992).  

 

  15  

Using   the   thyroid   metabolism   as   an   example,   one   can   hypothesize   how   genetic   changes   actually  

induce   the   alterations   we   see   from   wild   to   domesticated   phenotype.   The   thyroid   hormone  

metabolism  plays  a  crucial  part  in  the  ontogeny,  and  the  regulation  of  the  hormones  is  so  delicate  that  

even   minor   alterations   might   cause   profound   changes   in   physiological   and   behavioural   profiles  

(Crockford,  2002).  Still,  though  the  thyroid-­‐controlled  ontogeny  in  wild  and  captive  animals  do  differ,  

the   hormonal   metabolism   still   functions   in   domesticated   animals;   domesticates   just   exhibit   a  

significant  lowered  thyroid  secretion,  which  is  still  sufficient  to  produce  the  various  physiological  and  

cognitive  changes  that  we  see  in  domesticated  animals.  An  alteration  of  the  functional  parts  of  these  

genes   therefore   seems   less   likely.   Based   on   this,   it   is   tempting   to   assume   that   the   differences   in  

thyroid   synthesis   between   wild   and   domesticated   animals   should   be   found   in   differences   in  

components   involved   in   gene   expression.   This   means   that   domestication   potentially   could   be   the  

result  of  the  alteration  of  the  non-­‐coding  part  of  only  a  small  number  of  regulatory  genes  that  have  

their  effect  on  early  development  resulting   in   increased  taming  capacity  (Crockford,  2002;  Dobney  &  

Larson,  2006).  

 

                       4.1.2    Glucocorticoids  

The   hypothalamus   remains   a   key   component   in   adjusting   neuro-­‐endocrine   responses   according   to  

altered  environmental  scenarios.  As  domesticates  must  be  considered  to  live  in  a  less  extreme  and  a  

less  changeable  environment  when  compared  to  their  wild  ancestors,  it  seems  reasonable  to  suggest  

that   this   has   changed   the   selection   pressure   in   domesticates.     This   in   turn   could   hold   part   of   the  

explanation   for   the   altered   neuro-­‐endocrine   gene   expression   in   domesticates   (Saetre   et   al.,   2004).  

Lowered   levels   of   glucocorticoids   have   been   established   in   various   species   when   comparing  

individuals  displaying   tame  and  non-­‐tame  behaviour.  A   study  on  mink,  with   two  strains   selected   for  

“fearfulness”  and  “confidentiality”  respectively,  showed  that  though  the  individuals  of  the  two  strains  

had  the  same  capacity  to  secrete  cortisol,  fearful  mink  exhibited  significantly  higher  plasma  levels  than  

the  confident  mink  in  a  adrenocorticotropic  hormone  challenge  test  (Price,  2002).  Similar  results  have  

  16  

been   found   in   silver   foxes   (Vuples   vulpes)   methodically   bred   for   tame   or   non-­‐tame   behaviour   for  

generations   (Trut   et   al.,   2004).   In   a   study   where   15   animals   from   generation   35-­‐40   from   the   tame  

population   were   compared   with   15   animals   from   the   25th   to   30th   generation   from   the   non-­‐tame  

population,  plasma  levels  of  ATCH  and  cortisol  were  measured  and  compared  in  a  handling  situation.  

Results  showed  that  foxes  bred  for  tame  behaviour  displayed  a  significantly   lowered  level  of  plasma  

ATCH  and  cortisol  when  compared  to  the  non-­‐tame  population  (Gulevich  et  al.,  2004).  Furthermore,  

domesticates   also   show   attenuated   activity   of   hypothalamic-­‐pituitary-­‐adrenal   (HPA)   responses;  

animals   exhibiting   tameness   have   higher   plasma   concentrations   of   serotonin,   which   manifests   in  

lowered  aggression  (Popova  et  al.,  1991;  Trut  et  al.,  2004;  Trut  et  al.,  2009;  Hare  et  al.,  2012).      

 

The   established   interaction   between   glucocorticoids   and   neurotransmitters   only   emphasizes   the  

influence   the   alterations   of   these   hormonal   systems   have   on   behaviour   and   in   turn   domestication  

(Price,   2002).   It   seems   reasonable   to  assume   that  attenuated  plasma  hormonal   levels  of  mothers   in  

domesticated   species  will   have   an   effect   on   offspring   already   in   the   prenatal   state   (Francis,   1999).  

However,  indications  that  postnatal  maternal  behaviour  might  also  affect  the  expression  of  hormonal  

responses   to   stress   in  offspring  have  been   found   (Francis,   1999;  Price,   2002).    Mothers  will   differ   in  

their  frequency  and  quality  on  displayed  maternal  behaviour,  and  variation  in  maternal  behaviour  has  

been   indicated   to   be   individually   stable   across   litters/offspring   and   furthermore   to   correlate   to   the  

future  maternal   behaviour   in   daughters   (Fairbanks,   1989;  Meaney,   2001).   A   study   on   domestic   rats  

(Rattus  norvegicus)  showed  an  inverse  relationship  between  the  frequency  of  maternal  behaviour  and  

the   offsprings’   HPA-­‐mediated   response   to   stressful   situations   in   later   life.   But   this   relationship   also  

applied  to  the  quality  of  maternal  behaviour  given  to  the  offspring  when  they  were  young;  mothers  

primarily   assuming   a   sitting   position   with   their   backs   arched   and   the   hind   legs   to   the   side   when  

nursing  her  pups,   raised  offspring  with  a   lowered  HPA-­‐mediated   response   later   in   life   than  mothers  

primarily  nursing  their  pups  lying  down.  An  arched  back  posture  when  nursing  provide  the  pups  with  

  17  

more   flexibility   in   terms   of   nipple   switching   etc.,   and   is   thus   considered   to   be   a   higher   quality   of  

nursing  than  when  the  mothers  lie  down  (Meaney,  2001).  

 

Another   study   illustrating   how   alterations   of   hormonal   profiles   changes   the   behaviour   of  

domesticated  animals,  was  done  by  comparing  domestic  guinea  pigs   (Cavia  pocellus)  with   their  wild  

ancestor  the  cavy  (Cavia  aperea)  (Künzl  &  Sachser,  1999).  Seven  groups  of  adult  domestic  guinea  pigs  

and  five  groups  of  adult  wild  cavies  were  used  in  this  study.  Each  group  consisted  of  three  un-­‐related  

individuals;  one  male  and  two  females.  The  behaviour  of  the  animals  was  recorded  daily  throughout  a  

two-­‐week  period.  Furthermore,  during   the   two-­‐week  study  period,  males  were  subjected  to  a  novel  

arena   test   and   blood   samples  were   taken   before,   during   and   after   the   test   for   hormonal   analyses.  

Results   showed   that   the   domestic   guinea   pigs   and   the   wild   cavies   showed   the   same   behavioural  

repertoire,   but   the   wild   cavies   showed   significantly   more   aggressive   behaviour   compared   to   the  

domestic   guinea   pigs,   and   the   domestic   guinea   pigs   showed   significantly   more   socio-­‐positive  

behaviour  than  the  wild  cavies.  Wild  cavy  males  and  domestic  guinea  pig  males  had  the  same  baseline  

level   of   serum   concentrations   of   cortisol,   but   in   the   novel   arena   test,   the   wild   cavies   showed   a  

significantly  increased  stress  response  compared  to  the  domestic  guinea  pigs.  Furthermore,  domestic  

guinea  pig  males  displayed  significantly  higher   levels  of  courtship  behaviour  and  serum  testosterone  

concentrations  than  the  wild  cavy  males.  These  results  are  in  accordance  with  the  general  consensus  

that  domestication  leads  to  lowered  aggression,  lowered  stress  responses  and  increased  reproductive  

behaviour(Belyaev  et  al.,  1985;  Tchernov  &  Horwitz,  1991;  Jensen,  2006;  Künzl  &  Sachser,  1999;  Price,  

2002;  Zeder,  2012).  

 

 

 

 

 

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5. DOMESTICATION  OF  THE  DOG  

As  elaborated  below,  the  domestication  of  the  dog  turns  out  to  be  quite  a  unique  event.  In  spite  of  the  

obvious   lack   of   the   pre-­‐adaptational   traits   suggested   for   most   potential   (livestock)   domestic  

animals(Cameron-­‐Beaumont   et   al.,   2002;   Diamond,   2002;   Price,   2002;   Jensen,   2002;   Driscoll   et   al.,  

2009),  the  dog  remains  the  only  large  carnivore,  and  the  only  member  of  the  Canidae  family,  to  ever  

be  domesticated(Clutton-­‐Brock,  1995;  Wayne  &  vonHoldt,  2012).    

 

                       5.1      The  ancestral  origin  of  the  domestic  dog  

The  origin  of  the  domestic  dog  has  been  a  subject  of  great  discussion  through  time.  Given  the  extreme  

diversity  seen  in  domestic  dogs  many  scientists,  including  Darwin  (1859),  have  speculated  whether  the  

species   had   its   origin   in   one   or  multiple  wild   ancestral   species(   Scott   &   Fuller,   1965;   Clutton-­‐Brock,  

1995;  Klütsch  &  Savolainen,  2001;  Galibertet  al.,  2011).  Shared  haplotypes  and  successful  intra-­‐breeding  

events  among  various  species  in  the  canid  family  and  domestic  dogs  might  suggest  that  serveral  of  the  

38  present  canid  species  (Clutton-­‐Brock,  1995)  have  contributed  to  the  genetic  basis  of  the  domestic  

dog,  and  thus  portrays  a  more  complex  ancestry  than  just  a  single  species  origin.  Especially  the  jackal  

has  been  a  popular  candidate  when  speculating  about  possible  ancestors  (Clutton-­‐Brock,  1995;  Vila  &  

Wayne,   1999;   Dobney   &   Larson,   2006;   Galibert   et   al.,   2011).   However,   based   on   morphological,  

phylogenetic,   behavioural,   and   in   particular   molecular   genetic   analyses,   there   is   now   a   general  

consensus  that  the  grey  wolf  (Canis   lupus)   is  the  unique  ancestor  of  the  domestic  dog  (Morey,  1994;  

Vila  &  Wayne,  1999;  Klütsch  &  Savolainen,  2001;  Wayne  &  Vila,  2001;  Savolainen  et  al.,  2002;  Cooper  et  

al.,   2003;   Driscoll   et   al.,   2009;   Galibert   et   al.,   2011).   Still,   many   researchers   are   hypothesizing   that  

multiple  wolf  populations  and/or  backcrossing  events  after  initial  domestication  of  the  dog  can  explain  

the  extreme  diversity  we  see  in  the  more  than  400  dog  breeds  we  have  today  (Vila  et  al.,  1997;  Galibert  

et   al.,   2011).   However,   a   large   proportion   of   the   substantial   in-­‐between   breed   variation   could   be  

produced   by   a   relatively   modest   number   of   mutations.   Taking   into   account   how   many   possible  

combinations  only  a  few  handfuls  of  mutations  can  actually  produce,  this  might  be  enough  to  explain  

Part  II  

  19  

the  large  variety  we  see  within  the  domestic  dog  as  a  species  (Scott  &  Fuller,  1965;  Sutter  et  al.,  2007;  

Parker   et   al.,   2009;   Wayne   &   vonHoldt,   2012).   For   example,   the   morphological   phenotype  

chondrodysplasia,   which  we   see   as   the   short-­‐limbs   in   dog   breeds   such   as   dachshunds   and   corgies,  

derived  from  the  same  mutation  (Parker  et  al.,  2009;  Wayne  &  vonHoldt,  2012).  This  is  remarkable  as  

the  19  dog  breeds  displaying  chondrodysplasia  were  developed   in  several   independent  geographical  

locations  for  various  purposes,  and  genomics  analyses  of  their  populations’  structure  reveals  that  they  

in   fact  do  not   share  a   recent  common  ancestor   (Parker  et  al.,   2009).  Adding   to   that,   large  variation  

among   wolves,   both   between   populations   but   also   within   one   pack,   could   also   support   that   the  

potential   for   profound  within-­‐species   variation  might   have   been   latent   from   the   very   beginning   of  

domestication  of  the  dog  (Scott  &  Fuller,  1965).  

 

                       5.2    When  was  the  dog  domesticated?  

The   dog  was   by   far   the   first   animal   to   be   domesticated   (Klütsch  &   Savolainen,   2001;   Driscoll   et   al.,  

2009;   Galibert   et   al.,   2011;   Larson   et   al.,   2012).   Archaeological   findings   of   dog   remains   buried   with  

humans  date  back  to  the  Stone  Age  some  15,000  years  ago  (Morey,  1994;  Driscoll  et  al.,  2009;  Larson  

et   al.,   2012),   but   recent   evidence   obtained   from  genome-­‐sequencing   suggest   that   domestication   of  

the   dog  might   be  more   than   twice   as   old   dating   back   to   32,000   years   ago   (Wang   et   al.,   2013).   The  

finding  of  even  older  dog-­‐like  remains   in  Belgium,  suggests  an   incipient  dog  from  as  early  as  36,000  

years   ago   (Ovodov   et   al.,   2011).   Several   authors   even   mention   that   the   dog   could   have   been  

domesticated  more  than  100,000  years  ago  based  on  mtDNA  control  region  sequencing  showing  that  

the  monophyletic  clade  representing  the  domestic  dog  diverged  from  the  wolf  at  that  time  (Vila  et  al.,  

1997;  Diamond,  2002;  Dobney  &  Larson,  2006;).  The  mismatch  between  the  age  of  the  domestic  dog  

obviously   poses   some   problems.   Some   claim   that   using   archaeological   records   in   determining   the  

“when”  and  where”  in  the  earliest  dog  domestication  has  its  clear  weak  points  (Klütsch  &  Savolainen,  

2001).  Remains   are  often   incomplete   and   vary  greatly   in   frequency   and  quality  with  geography.   For  

instance,  soil  acidity   in  certain  areas  has  a  potentially   large  effect  on  the  quality  of  excavated  bones.  

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Furthermore,  determining  if  early  fossil  findings  are  wolf  or  a  dog  remains  can  prove  very  difficult.  For  

instance,  when  are  skull  proportions  different  enough  for  us  to  separate  between  ancestral  wolf  and  

early  domestic  dog  (Scott  &  Fuller,  1965;  Morey,  1994;  Klütsch  &  Savolainen,  2001;  Wayne  &  Vila,  2001)?  

Ovodov   et   al.   (2011)   object   to   this,   by   emphasizing   that   morphological   evidence   of   the   gradual  

characteristic  changes  making  a  wolf   into  a  dog  remains  the  single  most  reliable  criterion  to  tell   the  

two  relatives  apart.  Still,  even  though  some  find  it  questionable  whether  early  archaeological  findings  

are  actually  wolves  or  an  early  stage  of  domestic  dogs,  a  lot  of  these  fossil  remains  are  found  with  or  

in   close  proximity   to  human   fossil   settlements  and/or   remains.  This   suggests   that  early  humans  and  

wolves,   or  maybe  early   dogs,  were   living   close  enough   together   to   share   the   same   territories,   thus  

indicating  a  potential  preliminary  domestication  processes  was  already  in  effect  (Galibert  et  al.,  2011).      

 

                       5.3      The  geographical  origin  of  the  domestic  dog  

With   the   ancestral   heritage   settled,   the   geographical   origin   of   the   domestic   dog   remains   quite  

controversial  when  discussing  the  evolution  of  the  species.  There  is  a  profound  discrepancy  regarding  

this   subject,   and   the   lines   seem   to   be   drawn   rather   hard   between   the   scientists   who   believe   that  

Southern   East   Asia   is   the   geographical   origin   of   the   domestic   dog   (Klütsch   &   Savolainen,   2001;  

Savolainen  et  al.,  2002;  Pang  et  al.,  2009;  Ding  et  al.,  2012),  and  the  scientists  who  lead  our  attention  to  

Europe   and   the   Middle   East   (Verginelli,   2005;   vonHoldt   et   al.,   2010;   Galibert   et   al.,   2011;   Wayne   &  

vonHoldt,  2012)  as  the  possible  cradles  of  the  species.  As  no  final  conclusions  have  been  found  at  this  

time,  a  point  to  address  in  this  discussion  is  the  methods  used  for  analysing  genetic  material  to  reach  

consensus  on   the   geographical   origin   of   the  domestic   dog.   The   advocates   for   a   Southern   East  Asia  

origin   of   the   domestic   dog   (Klütsch   &   Savolainen,   2001;   Savolainen   et   al.,   2002;   Pang   et   al.,   2009)  

mainly   base   their   conclusions   on   genetic   analysis   obtained   from   mtDNA.   There   is   an   obvious   bias  

challenge  in  this  set  up,  as  mtDNA  is  solely  maternally  inherited.  Therefore,  mtDNA  analyses  might  be  

an  inadequate  estimator  of  which  individuals  actually  contributed  to  domestication,  and  furthermore,  

it  will  be  very  problematic  to  pick  up  on  backcrossing  events,  which  must  be  considered  to  be  a  very  

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likely  event  in  the  early  stages  of  dog  domestication  (Miklósi,  2007).  Furthermore,  the  markers  used  in  

mtDNA  analyses  are  only  approximately  15,000  base  pairs  long.  Thus,  conclusions  based  on  this  form  

of   mtDNA   can   possibly   be   considered   diluted   and   less   strong   (Vila   et   al.,   2005).   However,   recent  

evidence  using  a  14,437  bp  Y-­‐chromosome  DNA  sequence  sampled  in  151  dogs  around  the  world  shows  

a  similar  pattern  as  obtained  using  the  mtDNA  sequencing  and  thus  supports  the  belief  that  the  dog  

originated  from  Southern  east  Asia  (Ding  et  al.,  2012).    

The  researchers  arguing  Europe  and  the  Middle  East  to  be  the  possible  geographic  origins  of  domestic  

dogs  mainly  use  nuclearDNA  for  their  analyses  (Wayne  &  vonHoldt,  2012).  NuclearDNA  markers  have  

the   advantage   of   1)   being   considerably   larger,   and   2)   not   being   restricted   by  maternal   inheritance,  

which  could  lead  to  the  assumption  that  they  would  give  a  more  nuanced  and  precise  result.  However,  

too   increase   the   complexity   in   the  discussion   further,   some  authors   suggesting  a  Middle  Eastern  or  

European  origin  actually  do  use  mtDNA  analyses   to   reach   their   conclusions   (Verginelli,   2005).   Either  

way,  the  scientists  favouring  an  European  and/or  Middle  Eastern  origin  are  to  a  large  extent  supported  

by  archaeological  evidence  (Galibert  et  al.,  2011;  Ovodov  et  al.,  2011).    

 

While   this   seemingly   never-­‐ending  discussion   continues,   one  have   the  opportunity   to  wonder   if   the  

scenario  of  one  shared  origin  of  domesticated  dogs   in   fact   seems  a  bit  naïve.   It   seems  unlikely   that  

domestication  of  dogs  was  a  unique  event,  taking  place  in  a  single  isolated  location  in  the  world,  and  

much  more  likely  that  domestication  arose  from  various  geographical  locations  simultaneously  (Byrne,  

2005).  This  is  supported  by  the  fact  that  archaeological  evidence  tells  us  that  humans  and  wolves  co-­‐

existed  in  multiple  geographic  regions  during  the  late  Pleistocene(  Vila  et  al.,  1997;  Dobney  &  Larson,  

2006;).   Furthermore,   the   two   earliest   dogs   known   were   found   in   Belgium   and   Siberia.   They   are  

estimated  to  be  36,000  and  33,000  years  old  respectively,  and  the  very  early  dating  held  together  with  

the   large   geographical   separation   profoundly   points   in   the   direction   of   a   simultaneous   and   multi-­‐

regional  origin  to  the  domestic  dog  (Ovodov  et  al.,  2011).  

 

  22  

                       5.4      How  was  the  dog  domesticated?  

The  quite  over-­‐whelming  accumulation  of  controversies  of  “when”  and  “where”  in  domestication  of  

the   dog   leads   us   to   “how”   -­‐   which   turns   out   to   be   just   as   debated.   However,   based   primarily   on  

archaeological   evidence,   there   is   a   general   agreement   (for   now)   that   the  dog  was  domesticated  at  

least   15,000   years   ago  during   the  Mesolithic   period,  were   humans   lived   in   nomadic   hunter-­‐gatherer  

societies  with  a  geographical  overlap  with  wolf  populations  (Coppinger  &  Coppinger,  2001;  Price,  2002;  

Miklósi,  2007;  Driscoll  et  al.,  2009;  Morey,  2010;).  Various  theories  on  how  dogs  became  domesticated  

have  been  proposed.   They   are   all   based  on   a   variety   of   selection  hypotheses,   and   are  more  or   less  

convincing   in   their   outlines   of   how  wolves   transformed   into   the   domesticated   dog.   The   two  most  

popular  theories  involve  1)  individual-­‐based  selection  and  2)  population-­‐based  selection  (Miklósi,  2007;  

Morey,  2010).    

 

Humans   from   the   time   of   initial   stages   of   dog   domestication   would   be   co-­‐existing   with,   and  

encounter,   wolves   on   a   regular   basis   (Clutton-­‐Brock,   1995;   Miklósi,   2007;   Morey,   2010).   The   main  

argument  in  the  individual-­‐based  selection  theory  is  that  humans  initially  did  not  see  wolves  as  possible  

hunting  companions  and  guard  dogs,  but  simply  as  a  clothing-­‐  and  food  source.  Pups  in  a  den  are  very  

vulnerable   and   it   is   thus   hypothesized   that   humans   took   wolf   pups   straight   from   their   dens   for  

consumption  purposes  (Clutton-­‐Brock,  1995).  Just  as  Balyaev  found  it  in  his  initial  process  of  choosing  

individuals  for  the  founder  population  of  the  farm  fox  study  (Trut  et  al.,  2009;  Morey,  2010),  some  of  

these  pups  would  likely  have  displayed  a  more  docile  and  tame  behaviour  than  others,  and  those  pups  

might  have  been  spared  and  kept  within  the  human  settlement  and  socialized.    As  the  usefulness  of  

these   animals   for   other   purposes   than   food   probably   became   more   and   more   evident,   individuals  

continuously  displaying  desirable   features   in  behaviour  and   temperament   likely  became  subjects   for  

selective  breeding  over  multiple  generations  and  the  wild  wolf  gradually  and  very  slowly  turned  into  

the  domestic  dog  (Clutton-­‐Brock,  1995;  Miklósi,  2007).  Advocates  of  this  theory  points  to  the  fact  that  

we  see  wide  behavioural  spans  and  distinctions  among  pups  of  wild  canids,  and  that  some  individuals  

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should  be  more  suitable  for  domestication  than  others;  i.e.  the  capacity  for  taming  varies  in  a  litter  of  

wild   pups   and   some   pups   are   more   tame   than   others.   In   other   words,   they   are   in   a   rough  

interpretation   of   the   concept   “pre-­‐adapted   for   domestication”   (Price,   2002;   Miklósi,   2007;   Morey,  

2010).     The   existence   of   stabile   and   individual   behavioural   differences   have   been   shown   in   a   wide  

range  of  species  from  hermit  crabs  (Dardanus  calidus)  to  swift  foxes  (Vulpes  velox)  (Bremner-­‐Harrison  

et  al.,  2004;  Sih  et  al.,  2004;  Svartberg  et  al.,  2005;  Briffa  et  al.,  2008;  Sinn  et  al.,  2008;  Wolf  &  Weissing,  

2012),   but   most   studies   on   the   subject   have   been   conducted   on   adult   individuals.   Studies   on   such  

features   in   juvenile   individuals  are  sparse,  and   indications   that   individual  behavioural   traits  are  more  

plastic  in  juvenile  individuals  when  compared  to  adult  individuals  have  been  found  (Sinn  et  al.,  2008).  

However,   studies  on  wolf  pups  suggest   that   individual  behavioural  differences  do  become  stabile   in  

the  juvenile  stage  (Mac  Donald  &  Ginsburg,  1981;  MacDonald,  1983).  In  one  study  (MacDonald,  1983),  a  

litter  of  five  male  wolf  pups  were  raised  with  their  mother  in  captivity  for  the  first  four  weeks  of  their  

life.   At   four   weeks   of   age,   the   pups   were   taken   from   their   mother   and   group   housed.   The   pups  

underwent  extensive  behavioural  testing  already  from  17  days  of  age.  When  the  pups  reached  44  days  

of   age   a   cyclic   schedule   consisting   of   five   periods   of   no   testing   and   five   periods  with   testing  were  

introduced.  Non-­‐testing  periods  lasted  approximately  two  weeks  each,  and  here  the  litter  was  broken  

up  and  pups  were  in  turn  housed  paired  or  in  isolation.  Testing  periods  were  approximately  one  week  

long,  in  which  pups  were  housed  as  a  litter.  Throughout  the  test  periods,  various  test  types  were  used  

to  test  stability  in  individual  behavioural  traits;  novel  object  tests  together  as  a  litter  and  as  individuals,  

unfamiliar   person   tests   and   a   bone   competition   test.   The   results   showed   that   already   from   day   30  

there  was  a  clear  pattern  of  which  pup  would  repeatedly  claim  the  bone  in  the  bone  competition  test,  

and  from  day  44  a  stabile  individual  boldness  score  in  the  novel  object  tests  throughout  the  litter  was  

evident.   The   conclusion   of   the   study   was   that   early   variability   in   the   form   of   stabile   individual  

behavioural   differences   was   present   in   this   litter   of   wolf   puppies;   individual   behavioural   patterns  

became  stabile  already  around  day  44  of  age  and  showed  very  little  variance  hereafter.  Furthermore,  

the   study   suggests,   due   to   the   cyclic   discontinued   environmental   setting   for   the   pups   during   the  

  24  

study,   that   environmental   continuity   is   not   a   necessity   for   the   development   of   stabile   individual  

behavioural  differences.  In  another  study  (Mac  Donald  &  Ginsburg,  1981),  wolf  pups  were  raised  under  

various   restricted   conditions,   and   still   displayed   clear   individual   behavioural   differences,   which   the  

authors  even  determined  to  be  exaggerated  at  an  early  stage  due  to  the  restricted  upbringing.  These  

studies   supports   the   argument   used   by   those   in   favour   of   the   individual-­‐based   selection   theory;  

namely   that   early   individual   behavioural   differences   in   wolf   pups,   might   have   led   to   the   very   first  

selection  initiatives  on  the  way  to  creating  the  domestic  dog.  

 

The   population-­‐based   theory   suggests,   that   human   settlements   created   a   new   niche   for   wolves   in  

terms   of   an   easy   food   supply   in   discarded   food   and   other   waste.   Less   timid   wolves   successfully  

exploited  this  new  niche  by  living  as  scavengers,  gradually  tolerating  a  closer  proximity  to  humans  by  

displaying  an  increasingly  lowered  flight-­‐distance.  In  time,  these  animals  gained  a  selective  advantage  

over   the  wolves   not   exploiting   the   new   found   resource   (Coppinger  &   Coppinger,   2001;   Price,   2002;  

Miklósi,   2007;   Driscoll   et   al.,   2009;   Morey,   2010;).   This   phenomenon   is   described   as   proto-­‐

domestication;   a   natural   speciation   process   in   which   wild   animals   themselves   found   populations  

consisting  of  descendants  with  modified  phenotypes  (Crockford,  2002;  Galibert  et  al.,  2011).  The  result  

is   “primitive  natural  domesticates”  which   show  higher   levels  of  pre-­‐adaption   to  domestication   than  

un-­‐modified  conspecifics.  Other  authors  refer  to  this  process  as  self-­‐domestication  (Hare,  2002).  The  

proto-­‐domestication  would  then  be  followed  up  with  conscious  artificial  selection  for  desirable  traits,  

once   humans   realized   the   gain   in   domesticating   dogs   (Coppinger   &   Coppinger,   2001;   Price,   2002;  

Driscoll  et  al.,  2009;).    

   

Coppinger   &   Coppinger   (2001)   argues   that   the   individual-­‐based   selection   theory   requires   that   our  

human  ancestors  either  understood  the  usefulness  of  dogs  and/or  desired  them  as  pets.  The  question  

is,  according  to  Coppinger  &  Coppinger,  whether  Mesolithic  people  had  the  knowledge  to  engage  in  

the   ambitious   process   that   directional   selection   is;   how   could   they?   They   had   no   references.  

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Furthermore,   the   authors   emphasize   that   dog-­‐like   variation   is   not   present   in  wild  wolf   populations  

today  and  thus  assumedly  was  not  present  in  the  Mesolithic  period  either.  With  the  lack  of  variation,  

how  could   they  select   for   it?  Even   if  our  ancestors   indeed  did   see  a  potential   in   taming  wild  wolves  

through  even  the  slightest  variation  in  the  population,  the  authors  find  it  highly  questionable  that  they  

had  the  pre-­‐disposition  to  meticulously  select  for  these  vague  differences  generation  after  generation.  

And  wolves  presumably  do  not  make  good  pets.  Even  with  extensive  socialization,  hand-­‐reared  wolf  

pups   have   been   shown   to   have   significantly   lower   attachment   to   their   human   caregivers   when  

compared  to  dog  pups  reared  under  the  same  conditions  (Topál  et  al.,  2005).   Indications  have  been  

found  that  the  socialization  period  in  wolf  pups  is  both  shorter  and  more  rigid  than  in  dog  pups,  and  

missing   the  window  of  opportunity   in   terms  of   socialization   in  wolf   pups   seems   to  be  more  or   less  

irreversible  (Trut  et  al.,  2004;  Topál  et  al.,  2005).  Furthermore,  wolves  are  hard  to  contain  and  hard  to  

train   (R.   Coppinger   &   Coppinger,   2001).   However,   authors   (Hope,   1994;   R.   Coppinger   &   Coppinger,  

2001)   do  point   to   the   fact,   that   in   the   juvenile   stage,   both  pure-­‐breed  wolves   and  wolf-­‐dog  hybrids  

display  a  playful  and  pleasant  behaviour   towards  humans   if   socialized  correctly.  However,   the   idyllic  

picture  undergoes  a  very  radical  change  once  sexual  maturity  sets  in  in  these  animals  at  about  2  years  

of   age;   they   fulfil   their   genetic   disposition   and   become   the   pack-­‐oriented,   wide-­‐ranging   and   highly  

territorial  predators  they  really  are.  In  the  case  of  wolf-­‐hybrids,  the  clash  of  dog  and  wolf  behavioural  

features   can   prove   especially   problematic;  while   the   hybrid   displays   an   increased   level   of   tameness  

towards   humans   its   predatory   instincts   remains   relatively   intact   (Price,   2002).   Estimates   from   the  

Humane  Society  in  the  United  States,  paints  the  sinister  picture  of  80-­‐90%  of  ownerships  of  wolf-­‐dog  

hybrids  ending  in  failure  before  the  hybrid  reaches  the  age  of  3  years.  The  outcome  is  often  fatal  to  the  

hybrid,  being  abandoned  or  euthanized  (Hope,  1994).      

 

With  the  above  in  mind,  one  can  only  wonder  if  keeping  wolves  would  be  desirable  to  our  forefathers,  

or   if   the   attempt   to   tame   single   wild   individuals   would   have   proven   successful   (R.   Coppinger   &  

Coppinger,  2001;  Price,  2002).  Belyaevs  legendary  study  (  Trut,  1998;  Trut,  1999;  Trut  et  al.,  2004;  Trut  

  26  

et   al.,   2009;)   arguably   provides   support   for   the   individual-­‐based   selection   theory,   given   that   our  

ancestors  only  bred  individuals  displaying  pre-­‐adaptation  traits  for  domestication.  Belyaev  selectively  

bred  silver  foxes  solely  on  the  trait  “tameness”,  which  resulted  in  foxes  with  dog-­‐like  features  such  as  

wagging   tails,   floppy   ears   and   altered   coat   colours   in   only   4-­‐10   generations.   So,   individual-­‐based  

selection  can  be  done  with  surprisingly  fast  results.  But  applying  this  to  the  individual-­‐based  selection  

theory   raises   the   obvious   question   of   how   individual  wolves   displaying   tameness  were   successfully  

kept  and  contained  throughout  sexual  maturity  and   later   reproductive  stages.  Miklosi   (2007)  argues  

that  the  selective  breeding  of  wolves  was  not  the  first  stage  in  domestication  of  the  dog,  but  occurred  

once  initial  domestication  had  taken  place  as  a  selection  for  breeds  with  different  morphological  and  

behavioural  pre-­‐dispositions.  But  then  we  are  still  left  with  a  missing  piece  in  the  puzzle:  how  did  initial  

domestication  take  place?    

 

The   self-­‐domestication   process   in   the   population-­‐based   selection   theory   might   explain   initial  

domestication.   Some   critics   of   this   theory   believe   that   domestication   only   took   place   in   a   few  

geographical  locations,  and  raise  the  question  whether  it  thus  seem  likely  that  multiple  places  where  

humans  and  wolves   lived  together  only  resulted   in  a  handful  of  origins  to  domestication  of  the  dog.  

Another   objection   to   the   population-­‐based   selection   theory   is   that   in   a   hunter-­‐gatherer   society  

enough   food  waste  was   not   produced   to   sustain   a   larger   group  of   scavenging  wolves.   They  would  

need   to   hunt   as   a   supplement,   thereby   losing   their   selective   advantage   of   switching   to   a   strict  

scavenger   diet   (Miklósi,   2007).   Ovodov   et   al.   (2011)   suggest   what   could   be   an   important   fact,   and  

possible  explanation,   for  the  great  controversy  of  the  geographical  origin  of  the  domestication  dog;  

domestication  depended  on  several  concurrent  conditions  to  be  fulfilled,  and  it  thus  seems  likely  the  

process  would   have   failed   on   numerous   occasions   before   it  was   complete.   The   authors   are   strong  

supporters  of  the  theory  of  multiple  origins  of  the  domestic  dog  brought  about  by  self-­‐domestication.  

However,   they   also   emphasize   that   certain   aspects   of   human   activity,   such   as   hunting   techniques,  

food   surplus   and   a   rather   permanent   settlement   in   an   otherwise   nomadic   time   period,   all   were  

  27  

criterias   to   initiate   the   self-­‐domestication   process.   If   dog   domestication   indeed   was   a   process  

dependent  on  multiple   factors,   and   the   ideal   conditions   in   fact  were  present,   they  might  only   have  

existed   for   a   short   time,   not   producing   anything   but   modified   wolves   with   some   dog-­‐like  

characteristics.   Adding   to   this,   Crockford   (in   Morey,   2010)   acknowledge   that   proto-­‐domestication  

probably   happened   on   multiple   occasions,   thus   supporting   the   theory   that   domestication   was  

initiated  serveral  times  by  wild   living  wolves  themselves  through  self-­‐domestication,  but  the  process  

often  failed  in  these  early  stages.  

 

At  the  end  of  the  day,  these  two  very  different  domestication  theories  do  have  some  common  ground;  

they  both  boil  down  to  the  fact  some  wolves  were  more  tolerant  towards  humans  than  others.  Why  

was   that?   Suggestive   answers   leads   us   back   to   the  big  wheel   of   alterations  of   the   neuro-­‐endorcine  

system   (Crockford,   2002):   the   sympathetic   adrenal   gland   function   is   controlled   by   adrenergic  

receptors  and  adrenergic  receptors  are  in  turn  under  strong  influence  of  thyroid  hormone  levels.  Thus  

thyroid  hormones  are  directly  controlling  the  stress  response  in  animals.  Animals  (wild  and  domestic)  

display  variation  in  thyroid  metabolism  both  on  interspecific  and  intraspecific  levels,  which  means  that  

there  will  be  variations   in  stress   responses  across  populations  and  species.  This  could  be  a  plausible  

explanation;  both  entire  populations  and  single  wolves  displaying  a  higher  stress-­‐tolerance  would  be  

better  adapted  to  the  novel  environment  human  settlements  created.  This  in  turn  could  have  created  

a   population   of   proto-­‐domesticated   animals   that   later   were   subject   for   artificial   selection   (Morey,  

2010).  In  connection  to  the  earlier  paragraph  on  the  proven  neuro-­‐endocrine  changes  in  domesticated  

animals,  this  theory  makes  a  rather  convincing  argument.  Thus  wolves  displaying  attenuated  thyroid  

hormone  profiles  might  have  founded  the  domestic  dog  (Crockford,  2002)  

 

6. CONCLUSION  

The   domestication   process   started   a   cascade   of   events   that   gradually   changed   wild   animals   in   to  

animals  that  we  could  use  for  food,  transportation,  recreation  and  company.  The  desirable  behaviour  

we  consciously  select  for  in  our  domesticated  animals  originates  in  basic  changes  in  neuro-­‐endocrine  

  28  

pathways,  which  has  lead  to  further  alterations  of  morphology  and  physiology.  The  fascinating  study  

started  by  Belyaev  back  in  the  1950’s  illustrates  the  domestication  process  and  all  the  changes  it  brings  

with   it,   by   only   selective   for   one   single   behavioural   trait.   This   emphasizes   how   important   a   role  

behaviour  must  have  played  in  the  animals  founding  domesticated  populations,  and  how  these  valued  

behaviours  were  recognized  by  our  forefathers  thousands  of  years  ago.  

 

There   are   still   many   unanswered   questions   about   the   domestication   process,   and   particular   in   the  

domestication  of  the  dog.  The  seemingly  unlikely  event  of  successfully  domesticating  a  large  carnivore  

as  the  wolf  also  happened  to  be  the  very  first  event  of  domestication,  and  the  subject  fascinates  many  

scientists.   As   our  methods   for   tracking   such   events   back   in   time   improve,   we   get   a   little   closer   to  

answering  the  questions  we  so  vividly  discuss  about  how,  when  and  where  the  dog  was  domesticated.  

It  might  seem  more  likely  that  we  eventually  will  learn  the  answer  about  the  geographical  origin  of  the  

dog,  and  with  it  how  old  the  dogs  is  a  species,  than  how  the  dog  was  domesticated.  While  Belyaev  has  

provided  us  with   the  evidence   for  a  possible   rapid  domestication  process  by  selecting   for   tameness  

alone,  the  initial  process  remains  puzzling  and  very  hard  to  answer.  With  the  event  of  domestication  of  

the  dog  lies  15,000  or  more  years  back  in  time  obtaining  clues  of  how  this  process  started  are  difficult  

to   obtain.   However,   increasing   our   knowledge   and   understanding   of   the   behavioural   differences  

between  wolves  and  dogs  might  be  a  start.  

 

 

7. REFERENCES  

 Albert,  F.  W.,  Shchepina,  O.,  Winter,  C.,  Römpler,  H.,  Teupser,  D.,  Palme,  R.,  et  al.  (2008).  Phenotypic  differences  in  behavior,  

physiology   and   neurochemistry   between   rats   selected   for   tameness   and   for   defensive   aggression   towards   humans.  Hormones  and  Behavior,  53(3),  413–421.    

 Belyaev,   D.   K.,   Plyusnina,   I.   Z.,   &   Trut,   L.   N.   (1985).   Domestication   in   the   silver   fox   (Vulpes   fulvus   Desm):   Changes   in  

physiological  boundaries  of  the  sensitive  period  of  primary  socialization.  Applied  Animal  Behaviour  Science,  13,  359-­‐370.    Bremner-­‐Harrison,  S.,  Prodohl,  P.  A.,  &  Elwood,  R.  W.  (2004).  Behavioural  trait  assessment  as  a  release  criterion:  boldness  

predicts  early  death  in  a  reintroduction  programme  of  captive-­‐bred  swift  fox  (Vulpes  velox).  Animal  Conservation,  7(3),  313-­‐320.  

 Briffa,   M.,   Rundle,   S.   D.,   &   Fryer,   A.   (2008).   Comparing   the   strength   of   behavioural   plasticity   and   consistency   across  

situations:   animal   personalities   in   the   hermit   crab   Pagurus   bernhardus.   Proceedings,   the   Royal   Society,   Biological  Sciences,  275(1640),  1305-­‐1311.  

 Bruford,  M.  W.,  Bradley,  D.  G.,  &  Luikart,  G.  (2003).  DNA  markers  reveal  the  complexity  of   livestock  domestication.  Nature  

Reviews.  Genetics,  4(11),  900–910.      Byrne,  R.  W.  (2005).  Animal  Evolution:  Foxy  Friends.  Current  Biology,  15(3),  86-­‐87.    Byrne,   R.  W.,   &   Corp,   N.   (2004).   Neocortex   size   predicts   deception   rate   in   primates.   Proceedings   of   the   Royal   Society   of  

London  B:  Biological  Sciences,  271(1549),  1693–1699.        

  29  

Cameron-­‐Beaumont,   C.,   Lowe,   S.   E.,   &   Bradshaw,   J.   W.   S.   (2002).   Evidence   suggesting   preadaptation   to   domestication  throughout  the  small  Felidae.  Biological  Journal  of  the  Linnean  Society,  75(3),  361–366.  

   Clutton-­‐Brock,  J.  (1992).  The  process  of  domestication.  Mammal  Review,  22(2),  79–85.    Clutton-­‐Brock,   J.   (1995).   The   Domestic   Dog:   Its   Evolution,   Behaviour   and   Interactions   with   People.   The   Domestic   Dog:   Its  

Evolution,  chapter  2.  Cambridge  University  Press.    Cooper,   J.   J.,   Ashton,   C.,   Bishop,   S.,   West,   R.,   Mills,   D.   S.,   &   Young,   R.   J.   (2003).   Clever   hounds:   social   cognition   in   the  

domestic  dog  (Canis  familiaris).  Applied  Animal  Behaviour  Science,  81(3),  229–244.      Coppinger,   R.,   &   Coppinger,   L.   (2001).   Dogs:   A   New  Understanding   of   Canine  Origin,   Behavior   &   Evolution.   University   of  

Chicago  Press,  2nd  edition.    Crockford,  S.  J.  (2002).  Animal  domestication  and  heterochronic  speciation.  Human  Evolution  Through  Developmental  Change,  

chapter  6.  The  Johns  Hopkins  University  Press.    Darwin  C.  (1859).  The  origin  of  species.    London:  Murray  

Diamond,  J.  (2002).  Evolution,  consequences  and  future  of  plant  and  animal  domestication.  Nature,  418(6898),  700–707.      Ding,   Z.-­‐L.,   Oskarsson,   M.,   Ardalan,   A.,   Angleby,   H.,   Dahlgren,   L.-­‐G.,   Tepeli,   C.,   et   al.   (2012).  Origins   of   domestic   dog   in  

southern  East  Asia  is  supported  by  analysis  of  Y-­‐chromosome  DNA.  Heredity,  108(5),  507–514.    Dobney,  K.,  &  Larson,  G.  (2006).  Genetics  and  animal  domestication:  new  windows  on  an  elusive  process.  Journal  of  Zoology  

(269),  261-­‐271.    Driscoll,   C.   A.,   Macdonald,   D.   W.,   &   O'Brien,   S.   J.   (2009).   From   wild   animals   to   domestic   pets,   an   evolutionary   view   of  

domestication.  Pnas,  106(1),  9971–9978.    Dunbar,  R.  I.  M.,  &  Bever,  J.  (2010).  Neocortex  Size  Predicts  Group  Size  in  Carnivores  and  Some  Insectivores.  Ethology,  104(8),  

695–708.    Fairbanks,   L.   A.   (1989).   Early   experience   and   cross-­‐generational   continuity   of   mother-­‐infant   contact   in   vervet   monkeys.  

Developmental  Psychobiology,  22(7),  669–681.      Francis,   D.   (1999).   Nongenomic   Transmission   Across   Generations   of  Maternal   Behavior   and   Stress   Responses   in   the   Rat.  

Science,  286(5442),  1155–1158.    Galibert,   F.,  Quignon,   P.,  Hitte,   C.,  &  André,   C.   (2011).   Toward  understanding  dog  evolutionary   and  domestication  history.  

Comptes  Rendus  Biologies,  334(3),  190–196.      Gentry,  A.,  Clutton-­‐Brock,  J.,  &  Groves,  C.  P.  (2004).  The  naming  of  wild  animal  species  and  their  domestic  derivatives.  Journal  

of  Archaeological  Science  (31),  645-­‐651  .    Giuffra,   E.,   Kijas,   J.  M.   H.,   Amarger,   V.,   Carlborg,   Ö.,   Jeon,   J.   T.,   &   Andersson,   L.   (2000).   The   origin   of   the   domestic   pig:  

independent  domestication  and  subsequent  introgression.  Genetics  (154),  1785-­‐1791.    Goodwin,  D.,  Bradshaw,  J.  W.  S.,  &  Wickens,  S.  M.  (1997).  Paedomorphosis  affects  agonistic  visual  signals  of  domestic  dogs.  

Animal  Welfare  Information  Center  Newsletter  (USA),  53,  297–304.    Gulevich,   R.   G.,   Oskina,   I.   N.,   Shikhevich,   S.   G.,   Fedorova,   E.   V.,   &   Trut,   L.   N.   (2004).   Effect   of   selection   for   behavior   on  

pituitary–adrenal  axis  and  proopiomelanocortin  gene  expression  in  silver  foxes  (Vulpes  vulpes).  Physiology  and  Behavior,  82(2-­‐3),  513–518.  

 Hare,  B.  (2002).  The  Domestication  of  Social  Cognition  in  Dogs.  Science,  298(5598),  1634–1636.      Hare,  B.,  Wobber,  V.,  &  Wrangham,  R.  (2012).  The  self-­‐domestication  hypothesis:  evolution  of  bonobo  psychology  is  due  to  

selection  against  aggression.  Animal  Welfare  Information  Center  Newsletter  (USA),  83(3),  573–585.      Hemmer,  H.  (1990).  Domestication:  The  Decline  of  Environmental  Appreciation.  Cambridge  University  Press;  2  edition.    Hope  J.  (1994).  Wolves  and  wolf  hybrids  as  pets  are  big  business  but  a  bad  idea,  Smithsonian,  Volume  25:3  

  30  

 Jansen,  T.,  Forster,  P.,  Levine,  M.  A.,  Oelke,  H.,  Hurles,  M.,  Renfrew,  C.,  et  al.  (2002).  Mitochondrial  DNA  and  the  origins  of  

the  domestic  horse.  Proceedings  of  the  National  Academy  of  Sciences,  99(16),  10905–10910.      Jensen,  P.  (2002).  The  ethology  of  domestic  animals  -­‐  an  introductory  text.  CABI  Publishing.    Jensen,  P.  (2006).  Domestication—From  behaviour  to  genes  and  back  again.  Applied  Animal  Behaviour  Science,  97(1),  3–15.    Klütsch,  C.  F.,  &  Savolainen,  P.  (2001).  Geographical  Origin  of  the  Domestic  Dog.  In:  Encyclopedia  of  Life  Sciences  (ELS).  John  Wiley  &  Sons,  Ltd:  Chichester.

Kruska,  D.  (1988).  Mammalian  Domestication  and  its  Effect  on  Brain  Structure  and  Behavior  (pp.  211–250).  Berlin,  Heidelberg:  Springer  Berlin  Heidelberg.    

 Kruska,  D.  (1996).  The  effect  of  domestication  on  brain  size  and  composition  in  the  mink  (  Mustela  vison).  Journal  of  Zoology,  

239(4),  645–661.      Künzl,  C.,  &  Sachser,  N.  (1999).  The  Behavioral  Endocrinology  of  Domestication:  A  Comparison  between  the  Domestic  Guinea  

Pig  (Cavia  apereaf.porcellus)  and  Its  Wild  Ancestor,  the  Cavy  (Cavia  aperea).  Hormones  and  Behavior  (35),  28-­‐37.    Larson,  G.,  Karlsson,  E.  K.,  Perri,  A.,  Webster,  M.  T.,  Ho,  S.  Y.  W.,  Peters,  J.,  et  al.   (2012).  Rethinking  dog  domestication  by  

integrating   genetics,   archeology,   and  biogeography.  Proceedings   of   the  National   Academy   of   Sciences,   109(23),   8878–8883.    

 Mac  Donald,   K.   B.,   &   Ginsburg,   B.   E.   (1981).   Induction   of   normal   prepubertal   behaviour   in  wolves  with   restricted   rearing.  

Behavioral  and  Neural  Biology,  33,  133–162.    MacDonald,   K.   (1983).   Stability   of   individual   differences   in   behavior   in   a   litter   of   wolf   cubs   (Canis   lupus).   Journal   of  

Comparative  Psychology,  97(2),  99–106.      Meaney,  M.  J.  (2001).  Maternal  care,  gene  expression,  and  the  transmission  of  individual  differences  in  stress  reactivity  across  

generations.  Annual  Review  of  Neuroscience,  24,  1161–1192.      Mignon-­‐Grasteau,  S.,  Boissy,  A.,  Bouix,  J.,  Faure,  J.-­‐M.,  Fisher,  A.  D.,  Hinch,  G.  N.,  et  al.   (2005).  Genetics  of  adaptation  and  

domestication  in  livestock.  Livestock  Production  Science,  93(1),  3–14.      Miklósi,  Á.  (2007).  Dog  Behaviour,  Evolution,  and  Cognition.  Oxford  University  Press  Inc.    Morey,  D.  (2010).  Dogs:  Domestication  and  the  Development  of  a  Social  Bond.  Cambridge  University  Press.    Morey,  D.  F.  (1994).  The  early  evolution  of  the  domestic  dog.  American  Scientist,  82(4),  336–347.    Ovodov,  N.  D.,  Crockford,  S.  J.,  Kuzmin,  Y.  V.,  Higham,  T.  F.  G.,  Hodgins,  G.  W.  L.,  &  van  der  Plicht,  J.  (2011).  A  33,000-­‐year-­‐old  

incipient  dog  from  the  Altai  Mountains  of  Siberia:  evidence  of  the  earliest  domestication  disrupted  by  the  Last  Glacial  Maximum.  PLoS  ONE,  6(7),  e22821.    

 Pang,  J.-­‐F.,  Kluetsch,  C.,  Zou,  X.-­‐J.,  Zhang,  A.-­‐B.,  Luo,  L.-­‐Y.,  Angleby,  H.,  et  al.  (2009).  mtDNA  data  indicate  a  single  origin  for  

dogs  south  of  Yangtze  River,  less  than  16,300  years  ago,  from  numerous  wolves.  Molecular  Biology  and  Evolution,  26(12),  2849–2864.    

 Parker,   H.   G.,   vonHoldt,   B.   M.,   Quignon,   P.,   Margulies,   E.   H.,   Shao,   S.,   Mosher,   D.   S.,   et   al.   (2009).   An   expressed   fgf4  

retrogene  is  associated  with  breed-­‐defining  chondrodysplasia  in  domestic  dogs.  Science,  325(5943),  995–998.      Popova,  N.  K.,  Voitenko,  N.  N.,  Kulikov,  A.  V.,  &  Avgustinovich,  D.  F.  (1991).  Evidence  for  the  involvement  of  central  serotonin  

in  mechanism  of  domestication  of  silver  foxes.  Pharmacology,  Biochemistry,  and  Behavior,  40(4),  751–756.    Price,  E.  O.  (2002).  Animal  domestication  and  behaviour.  CABI  Publishing,    CAB  Int.,  1–307.    Saetre,  P.,  Lindberg,  J.,  Leonard,  J.  A.,  Olsson,  K.,  Pettersson,  U.,  Ellegren,  H.,  et  al.  (2004).  From  wild  wolf  to  domestic  dog:  

gene  expression  changes  in  the  brain.  Molecular  Brain  Research,  126(2),  198–206.      Savolainen,  P.,  Zhang,  Y.-­‐P.,  Luo,  J.,  Lundeberg,  J.,  &  Leitner,  T.  (2002).  Genetic  evidence  for  an  East  Asian  origin  of  domestic  

dogs.  Science,  298(5598),  1610–1613.      

  31  

Scott,  J.  P.,  &  Fuller,  J.  L.  (1965).  Genetics  and  the  social  behavior  of  the  dog  -­‐  the  classic  study.  University  of  Chicago  Press.      Sih,  A.,  Bell,  A.,  &  Johnson,  J.  C.  (2004).  Behavioral  syndromes:  an  ecological  and  evolutionary  overview.  Trends  in  Ecology  &  

Evolution,  19(7),  372–378.      Sinn,   D.   L.,   Gosling,   S.   D.,   &  Moltschaniwskyj,   N.   A.   (2008).   Development  of   shy/bold  behaviour   in   squid:   context-­‐specific  

phenotypes  associated  with  developmental  plasticity.  Animal  Behaviour  (75),  433-­‐442.  Sol,  D.,  Bacher,  S.,  Reader,  S.  M.,  &  Lefebvre,  L.  (2008).  Brain  size  predicts  the  success  of  mammal  species   introduced  into  

novel  environments.  The  American  Naturalist,  172  Suppl  1,  63–71.      Sol,  D.,  Duncan,  R.  P.,  Blackburn,  T.  M.,  Cassey,  P.,  &  Lefebvre,  L.   (2005).  Big  brains,  enhanced  cognition,  and  response  of  

birds  to  novel  environments.  Pnas,  102,  5460–5465.    Spady,  T.  C.,  &  Ostrander,  E.  A.  (2007).  Canid  genomics:  mapping  genes  for  behavior  in  the  silver  fox.  Genome  Research,  17(3),  

259–263.      Sutter,   N.   B.,   Bustamante,   C.   D.,   Chase,   K.,   Gray,   M.   M.,   Zhao,   K.,   Zhu,   L.,   et   al.   (2007).   A   single   IGF1   allele   is   a   major  

determinant  of  small  size  in  dogs.  Science,  316(5821),  112–115.      Svartberg,  K.,  Tapper,   I.,  Temrin,  H.,  Radesäter,  T.,  &  Thorman,  S.   (2005).  Consistency  of  personality  traits   in  dogs.  Animal  

Behaviour),  69(2),  283–291.      Tchernov,   E.,   &   Horwitz,   L.   K.   (1991).   Body   size   diminution   under   domestication:   Unconscious   selection   in   primeval  

domesticates.  Journal  of  Anthropological  Archaeology,  10,  54-­‐75.    Topál,  J.,  Gácsi,  M.,  Miklósi,  Á.,  Virányi,  Z.,  Kubinyi,  E.,  &  Csányi,  V.  (2005).  Attachment  to  humans:  a  comparative  study  on  

hand-­‐reared  wolves  and  differently  socialized  dog  puppies.  Animal  Behaviour,  70(6),  1367–1375.      Trut,  L.  (1999).  Early  Canid  Domestication:  The  Farm-­‐Fox  Experiment.  American  Scientist,  87(2),  160-­‐165.    Trut,  L.  N.  (1998).  The  evolutionary  concept  of  destabilizing  selection:  status  quo.  Journal  of  Animal  Breeding  and  Genetics,  115,  

415-­‐431    Trut,  L.  N.  (2001).  Experimental  studies  of  early  canid  domestication.  The  Genetics  of  the  Dog,  chapter  2.  CABI  Publishing.    Trut,  L.  N.,  Plyusnina,  I.  Z.,  &  Oskina,  I.  N.  (2004).  An  Experiment  on  Fox  Domestication  and  Debatable  Issues  of  Evolution  of  

the  Dog.  Russian  Journal  of  Genetics,  40(6),  644–655.    Trut,   L.,   Oskina,   I.,   &   Kharlamova,   A.   (2009).   Animal   evolution   during   domestication:   the   domesticated   fox   as   a   model.  

Bioessays,  31(3),  349–360.      Verginelli,   F.   (2005).  Mitochondrial   DNA   from   Prehistoric   Canids   Highlights   Relationships   Between   Dogs   and   South-­‐East  

European  Wolves.  Molecular  Biology  and  Evolution,  22(12),  2541–2551.      Vila,  C.  (2001).  Widespread  Origins  of  Domestic  Horse  Lineages.  Science,  291(5503),  474–477.      Vila,  C.,  &  Wayne,  R.  K.  (1999).  Hybridization  between  Wolves  and  Dogs.  Conservation  Biology,  13(1),  195–198.      Vila,  C.,  Savolainen,  P.,  Maldonado,  J.  E.,  Amorim,  I.  R.,  Rice,  J.  E.,  Honeycutt,  R.  L.,  et  al.  (1997).  Multiple  and  ancient  origins  

of  the  domestic  dog.  Science,  276(5319),  1687–1689.    Vila,   C.,   Seddon,   J.,   &   Ellegren,   H.   (2005).  Genes   of   domestic  mammals   augmented   by   backcrossing  with  wild   ancestors.  

Trends  in  Genetics,  21(4),  214–218.      vonHoldt,  B.  M.,  Pollinger,  J.  P.,  Lohmueller,  K.  E.,  Han,  E.,  Parker,  H.  G.,  Quignon,  P.,  et  al.   (2010).  Genome-­‐wide  SNP  and  

haplotype  analyses  reveal  a  rich  history  underlying  dog  domestication.  Nature,  464(7290),  898–902.      Wang,   G.-­‐D.,   Zhai,  W.,   Yang,   H.-­‐C.,   Fan,   R.-­‐X.,   Cao,   X.,   Zhong,   L.,   et   al.   (2013).   The   genomics   of   selection   in   dogs   and   the  

parallel  evolution  between  dogs  and  humans.  Nature  Communications,  4,  1860.    Wayne,  R.  K.,  &  Vila,  C.  (2001).  Phylogeny  and  origin  of  the  domestic  dog.  The  Genetics  of  the  Dog,  chapter  1.  CABI  Publishing.    

  32  

Wayne,  R.  K.,  &  vonHoldt,  B.  M.  (2012).  Evolutionary  genomics  of  dog  domestication.  Mammalian  Genome,  23(1-­‐2),  3–18.        Wolf,   M.,   &   Weissing,   F.   J.   (2012).   Animal   personalities:   consequences   for   ecology   and   evolution.   Trends   in   Ecology   &  

Evolution,  27(8),  452–461.      Zeder   MA.   (2012).   Pathways   leading   to   domestication.   Chp   9   in   Biodiversity   in   Agricultre:   Domestication,   Evolution   and  Sustainability.   Edited   by   Gepts   P,   Famula   TR,   Bettinger   RL,   Brush   SB,   Damania   AB,   McGuire   PE,   Qualset   CO.Cambridge  University  Press.