H i ul. R i v . ' 1998,', 73, p p . 203-266 p r in te d in the U n ited K ingdom © C am bridge P h ilosoph ica l Society 203

A revised six-kingdom system of life

T. CAVALIER-SM ITHEvolutionary B iology Programme, Canadian Institu te f o r Advanced Research, D epartm ent o f B o tany , U niversity o f B ritish Columbia, Vancouver, B C , Canada V 6 T I f 4

(.Received 27 M a rch 1 9 9 6 ; revised 15 D ecember 1 9 9 7 ; accepted 18 December 1997)

A B S T R A C T

A re v is e d s ix -k in g d o m sy s te m o f life is p r e s e n te d , d o w n to th e level o f in f r a p h y lu m . A s in m y 1983 sy stem B a c te r ia a r e t r e a te d as a s in g le k in g d o m , a n d e u k a ry o te s a r e d iv id e d in to o n ly five k in g d o m s : P ro to z o a , A n im a l ia , F u n g i , P la n ta e a n d C h r o m is ta . I n t e r m e d ia t e h ig h level c a te g o r ie s ( s u p e rk in g d o m , s u b k in g d o m , b r a n c h , in f ra k in g d o m , s u p c rp h y lu m , s u b p h y lu m a n d in f ra p h y lu m ) a r c e x te n s iv e ly u se d lo a v o id s p l i t t in g o rg a n is m s in to a n ex cess iv e n u m b e r o f k in g d o m s a n d p h y la (6 0 o n ly b e in g re c o g n iz e d ) . T h e tw o ‘ z o o lo g ic a l ’ k in g d o m s . P ro to z o a a n d A n im a l ia , a r e s u b je c t to th e I n t e r n a t io n a l C o d e o f Z o o lo g ic a l N o m e n c la tu r e , th e k in g d o m B a c te r ia to th e I n t e r n a t io n a l C o d e o f B a c te r io lo g ic a l N o m e n c la tu r e , a n d th e th r e e ‘ b o t a n i c a l ’ k in g d o m s ( P la n ta e , F u n g i , C h r o m is ta ) lo th e I n t e r n a t io n a l C o d e o f B o ta n ic a l N o m e n c la tu r e , C i r c u m s c r ip t io n s o f th e k in g d o m s B a c te r ia a n d P la n ta e r e m a in u n c h a n g e d s in c e C a v a l ic r - S m ith (1 9 8 1 ) . T h e k in g d o m F u n g i is e x p a n d e d b y a d d in g M ic ro s p o r id ia , b e c a u s e o f p r o te in s e q u e n c e e v id e n c e t h a t th e se a m ito c h o n d r ia l in t r a c e l lu la r p a r a s i te s a r e r e la te d to c o n v e n t io n a l F u n g i , n o t P ro to z o a . F u n g i a rc s u b d iv id e d in to fo u r p h y la a n d 2 0 c la sse s ; fu n g a l c la s s if ic a tio n a t th e r a n k o f su b c la ss a n d a b o v e is c o m p re h e n s iv e ly re v ise d . T h e k in g d o m s P ro to z o a a n d A n im a l ia a r e m o d if ie d in th e l ig h t o f m o le c u la r p h y lo g e n e t ic e v id e n c e th a t M y x o z o a a r c a c tu a l ly A n im a lia , n o t P ro to z o a , a n d t h a t m e so z o a n s a r c r e la te d lo b i l a te r ia n a n im a ls . A n im a l ia a re d iv id e d in to fo u r s u b k in g d o m s : R a d ia t a (p h y la P o r ife ra , C n id a r ia , P la c o z o a , C te n o p h o r a ) , M y x o z o a , M e s o z o a a n d B ila tc r ia ( b i la te ra l a n im a ls : a ll o th e r p h y la ) . S e v e ra l n e w h ig h e r lev e l g ro u p in g s a r e m a d e in th e a n im a l k in g d o m in c lu d in g th r e e n e w p h y la : A c a n th o g n a th a ( ro tife rs , a c a n th o c c p h a la n s . g a s tro tr ic h s , g n a th o s to m u l id s ) , B ra c h io z o a (b ra c h io p o d s a n d p h o ro n id s ) a n d L o b o p o d a ( o n y c h o p h o ra n s a n d ta rd i- g r a d e s ) , so o n ly 23 a n im a l p h y la a r e re c o g n iz e d . A r c h c z o a , h e r e r e s t r ic te d to th e p h y la M e ta m o n a d a a n d T r ic h o z o a , a r e t r e a te d as a s u b k in g d o m w ith in P ro to z o a , as in m y 1983 s ix -k in g d o m s y s te m , n o t as a s e p a ra te k in g d o m . T h e r e c e n t ly re v ise d p h y lu m R h iz o p o d a is m o d if ie d f u r th e r b y a d d in g m o re f la g e lla te s a n d re m o v in g so m e ‘ r h iz o p o d s ’ a n d is th e re fo re r e n a m e d C e rc o z o a . T h e n u m b e r o f p r o to z o a n p h y la is r e d u c e d b y g r o u p in g M y c e to z o a a n d A rc h a m o e b a e ( b o th n o w in f ra p h y la ) a s a n e w s u b p h y lu m C o n o s a w ith in th e p h y lu m A m o e b o z o a a lo n g s id e th e s u b p h y lu m L o b o sa , w h ic h n o w in c lu d e s b o th th e t r a d i t io n a l a e ro b ic lo b o se a n a m o e b a e a n d M u ltic ilia . H a p lo s p o r id ia a n d th e ( fo rm e r ly m ic ro s p o r id ia n ) m e lc h n ik o v c ll id s a re n o w b o th p la c e d w ith in th e p h y lu m S p o ro z o a . T h e s e c h a n g e s m a k e a to ta l o f o n ly 13 c u r r e n t ly r e c o g n iz e d p r o to z o a n p h y la , w h ic h a r c g ro u p e d in to tw o su b k in g d o m s : A r c h e z o a a n d N e o z o a ; th e la t io r is m o d ifie d in c i r c u m s c r ip t io n b y a d d in g th e D is c ic r is ta ta , a n e w in f ra k in g d o m c o m p r is in g th e p h y la P e rc o lo z o a a n d E u g le n o z o a ) . T h e s e c h a n g e s a re d isc u sse d in r e la t io n to th e p r in c ip le s o f m e g a s v s te m a tic s , h e r e d e f in e d as sy s te m a tic s t h a t c o n c e n t r a te s o n th e h ig h e r lev e ls o f c lasses, p h y la , a n d k in g d o m s . T h e s e p r in c ip le s a lso m a k e i t d e s i r a b le to r a n k A r c h a c b a c tc r ia a s a n in f ra k in g d o m o f th e k in g d o m B a c te r ia , n o t a s a s e p a ra te k in g d o m . A r c h a e b a c te r ia a r c g ro u p e d w ith th e in f ra k in g d o m P o s ib a c tc r ia to fo rm a n e w s u b k in g d o m , U n ib a c tc r ia , c o m p r is in g a ll b a c t e r i a b o u n d e d b y a s in g le m e m b r a n e . T h e b a c te r ia l s u b k in g d o m N e g ib a c te r ia , w ith s e p a r a te c y to p la s m ic a n d o u te r m e m b ra n e s , is s u b d iv id e d in to tw o in f ra k in g d o m s : L lp o b a c le r ia , w h ic h lack l ip o p o ly s a e c h a r id e a n d h a v e o n ly p h o s p h o l ip id s in th e o u te r m e m b r a n e , a n d G ly c o b a c .tc r ia , w i th l ip o p o ly s a c c h a r id e s in th e o u t e r le a f le t o f th e o u t e r m e m b r a n e a n d p h o s p h o l ip id s in Its in n e r le a f le t. T h is p r im a r y g r o u p in g o f th e 10 b a c te r ia l p h y la in to s u b k in g d o m s is b a s e d o n th e n u m b e r o f c c ll-c n v c lo p e m e m b ra n e s , w h ils t t h e i r su b d iv is io n in to in f ra k in g d o m s e m p h a s ise s th e i r m e m b r a n e c h e m is tr y ; d e f in i t io n o f th e n c g ib a c te r ia l p h y la , five a t le a s t p a r t ly p h o to s y n th e t ic , re lie s ch ie fly o n p h o lo s y n th e l ic m e c h a n is m a n d c c ll- c n v e lo p e s t r u c tu r e a n d c h e m is try c o r ro b o r a te d b y r ib o so m a l R N A p h y lo g e n y . T h e k in g d o m s P ro to z o a a n d C h r o m is ta a r e s lig h tly c h a n g e d in c ir c u m s c r ip t io n b y t r a n s f e r r in g s u b p h y lu m O p a l in a t a (c lasses O p a l in e a , P ro te ro m o n a d e a , B la s to c y s te a cl. n o v .) f ro m P ro to z o a in to in f ra k in g d o m H e te r o k o n ta o f th e

204 T . C a v a l i e r - S m i t h

kingdom C hrom ista . O p a lin a ta a rc g rouped w ith th e subphylum Pseudofungi and the zoofiagcllate Developayella elegans (in a new subphylum B igvrom onada) to form a new botanical phylum (Bigyra) of hctcro trophs w ith a double ciliary transitional helix, m aking it necessary to ab an d o n the phylum nam e

p h y lo g e n e t ic e v id e n c e .

Key w inds : M c g a s y s te m a tic s , B a c te r ia , P ro to z o a , A n th o z o a , F u n g i , A n im a lia , P la n ta e , C h r o m is ta , E u m y c o ta , M y c e to z o a .

C O N T E N T S

I . I n t r o d u c t i o n ................................................................................................................................................................................ 205I I . P h ilo so p h ic p r e l im in a r ie s .................................................................................................................................................... 2 1 0

11 ') D a r w in i a n e v o lu t io n a r y c la s s if ic a t io n c o n t r a s te d w i th H c n n ig i a n c la d i f ic a t io n ...................... 2 1 0(2) N a m in g t a x a a n d c l a d e s .......................................................................................................................................... 213(3) P r in c ip le s o f r a n k in g t a x a ....................................................................................................................................... 214(4) T h e n e e d to w e ig h a n d in te g r a te p h y lo g e n e t ic e v id e n c e f ro m d iv e rs e s o u r c e s ....................... 215

I I I . I n d e fe n c e o f B a c te r ia : th e so le p r im a ry k in g d o m o f life .................................................................................. 215(1) T h e c o n c e p t o f a b a c te r iu m ( sy n o n y m : p r o k a r y o t e ) ............................................................................. 215(2) C h a n g in g v ie w s o n A r c h a e b a c t e r i a .................................................................................................................... 216(3 ) T h e im p o r ta n c e o f c e ll s t r u c tu r e i n b a c te r i a l c la s s i f ic a t io n ................................................................ 217(4) C h a r a c te r s i m p o r t a n t in th e h ig h - le v e l c la s s if ic a tio n o f B a c t e r i a ................................................... 220(5) B a c te r ia l s u b k in g d o m s a n d in f r a k in g d o m s .................................................................................................... 222

IV . P ro to z o a , th e b a s a l e u k a r y o t ic k in g d o m .................................................................................................................... 226¡1) S ta tu s o f A r c h e z o a , e a r ly d iv e r g in g a m ito c h o n d r ia l e u k a r y o te s ..................................................... 2 2 6

(a) C h a n g e s in c ir c u m s c r ip t io n o f th e A r c h e z o a ....................................................................................... 226(2) T h e p r o to z o a n su b k in g d o m s : A r c h e z o a a n d N e o z o a ............................................................................. 229(3 ) D e m a r c a t io n b e tw e e n t h e tw o z o o lo g ic a l k in g d o m s : P ro to z o a a n d A n im a l i a ......................... 231(4) C la s s if ic a tio n o f th e N e o z o a ..................................................................................................................................... 234

(a) T h e in f ra k in g d o m S a r c o m a s t ig o ta ................................................................................................... 234(b) T h e in f ra k in g d o m A lv e o la ta ................................................................................................................ 238(r) T h e in f ra k in g d o m A d i n o p o d a ............................................................................................................ 238

V . T h e k in g d o m A n im a lia a n d its 23 p h y l a .................................................................................................................. 239(1) R a d ia ta , th e a n c e s t r a l a n im a l s u b k in g d o m ................................................................................................... 239(2 ) T h e d e r iv e d s u b k in g d o m M e s o z o a ..................................................................................................................... 2 3 9(3) T h e n u m b e r o f a n im a l p h y l a ................................................................................................................................ 239(4) A b r o a d e n e d p h y lu m A n n e l id a ............................................................................................................................ 240(5) T h e p s e u d o c o c lo m a tc p h y la N e m a th e lm in th c s a n d A c a n th o g n a th a p h v l . n o v ........................ 2 4 0(6) T h e n e w p h y la B ra c h io z o a a n d L o b o p o d a .................................................................................................. 241(7) P h y lo g e n e tic a s s u m p tio n s b e h in d th e n e w b i la te r ia n in f ra k in g d o m s a n d s u p e r p h y la 241(8) N e w a n im a l s u b p h v la a n d in f r a p h y la .............................................................................................................. 243

V I . T h e k in g d o m F u n g i a n d i t s fo u r p h y l a ..................................................................................................................... ‘244(1) C i r c u m s c r ip t io n o f th e F u n g i .................................................................................................................................. 244(2) T h e tr ic h o m y c c tc o r ig in o f m ic r o s p o r id ia ....................................................................... 245(3) R e v is io n o f h ig h e r fu n g a l c la s s i f ic a t io n ............................................................................................................ 245

V I I . T h e k in g d o m P la n ta e a n d its f iv e p h y l a .................................................................................................................. 249(1) N e w re d a lg a l s u b p h y l a ............................................................................................................................................ 249(2) N e w c h lo r o p h y tc i n f r a p h y la ................................................................................................................................... 251

V I I I . C h r o m is ta , th e t h i r d b o ta n ic a l k in g d o m , a n d its f iv e p h y l a .......................................................................... 251(1) M u l t ip le losses o f c h lo ro p la s ts b y c h r o m is t s ................................................................................................. 252¡2) T ra n s f e r o f O p a l i n a t a to C h r o m is ta : th e n e w h c lc r o k o n t p h y lu m B ig y r a ................................. 253(3) T h e o r ig in o f c i l ia ry r c l ro n c m c s a n d th e n a tu r e o f th e a n c e s tra l c h r o m is t .................................. 2 5 4(4) M i to c h o n d r ia l a n d c c ll- su r fa c e e v o lu t io n in c h ro m is ts ....................... .................................................. 255(5) R e tr o n e m e loss in O p a l i n a t a .................................................................................................................................. 256(6) A re th e r e o th e r u n id e n t i f ie d c h ro m is ts lu r k in g w i th in th e k in g d o m P ro to z o a l1....................... 257

A revised s ix -k in g d o m system o f life 205

I X . E n v o i .....................................................................................X . C o n c lu s io n s .........................................................................

X I . A c k n o w le d g e m e n ts ........................................................X I I . R e fe r e n c e s ............................................................................

I. IN T R O D U C T IO N

T h e id e a th a t n a tu r e c a n b e d iv id e d in to th re e k in g d o m s , m in e ra l , v e g e ta b le a n d a n im a l (L em ery , 1 6 75 ), w as p o p u la r iz e d b y L in n a e u s in th e e ig h te e n th c e n tu ry . A lth o u g h s e p a ra te k in g d o m s fo r fung i (N eck e r, 1783), P ro to z o a (O w e n , 1858) o r b a c te r ia (E n d e r le in , 1925) w e re p ro p o s e d la te r , th e seve n te e n th c e n tu ry c o n c e p tio n o f ju s t tw o k in g d o m s o f life d o m in a te d b io lo g y fo r th r e e c e n tu r ie s . T h e d is c o v e ry o f p ro to z o a (L e e u w e n h o e k , 1675) a n d b a c te r ia (L e e u w e n h o e k , 1683) e v e n tu a lly u n d e r m in e d th e tw o k in g d o m system . B u t g e n e ra l a g re e m e n t th a t th e liv in g w o rld m u s t b e classified in to a t le a s t five k in g d o m s (M a rg u lis & S c h w a r tz , 1988; C a v a lie r -S m ith , 1 9 8 9 a ; M a y r , 1990) w as re a c h e d o n ly a f te r th e d r a m a tic d isco v e rie s m a d e b y e lec tro n m ic ro sc o p y in th e seco n d h a lf o f th e tw e n tie th c e n tu ry . T h e se co n c lu s iv e ly c o n firm e d th e fu n d a m e n ta l d iffe ren ces b e tw e e n b a c te r ia a n d eu k a ry o te s , a n d re v e a le d th e tr e m e n d o u s u l t r a s t ru c tu ra l d i v e rs ity o f p ro tis ts . A c c e p ta n c e o f th e n ecess ity fo r se v e ra l k in g d o m s a lso ow es m u c h to th e sy s tem atic sy n th esis o f C o p e la n d (1956 ), a n d th e in f lu e n tia l w r it in g s o f S ta n ie r (1961 : S ta n ie r & v a n N ie i, 1962) a n d W h it ta k e r (1969).

W h e th e r m o re k in g d o m s th a n five a re n e e d e d (L c e d a le , 1974), a n d i f so h o w m a n y , h as b een d e b a te d fo r o v e r 20 y e a rs (C a v a lie r -S m ith , 1978, 1981 a ; M ö h n , 1984 ; C o rliss, 1994). E v en m o re im p o r ta n t th a n th e sh ee r n u m b e r o f k in g d o m s is th e fa c t t h a t th e d e fin itio n a n d c irc u m sc r ip tio n o f th e re c o g n iz e d k in g d o m s a re n o t y e t a g re e d by d if fe re n t sy s tem atis ts . P h y lo g e n e tic a d v a n c e s h a v e b e e n so g re a t o v e r th e p a s t 30 y ea rs , h o w ev e r, th a t w e c a n n o w d e fin e m o n o p h y ie tic k in g d o m s, th e c ir c u m sc r ip tio n o f w h ic h o u g h t to b e w id e ly a c c e p ta b le an d th e re fo re le a d to a m u c h d e s ire d s ta b il ity in th e m a c ro sy s te m o f life.

S o m e y ea rs ago , I a rg u e d th a t th e m in im u m n u m b e r o f k in g d o m s su ita b le fo r g e n e ra l p u rp o ses w as six (C a v a lie r -S m ith , 1981 a ) , a n d th a t in a d d it io n to th e p rev io u sly a c c e p te d five k in g d o m s it w as n ecessa ry to reco g n ize a th i rd b o ta n ic a l k in g d o m , C h ro m is ta (m a in ly c o m p r is in g th e oom ycetes a n d those n u m e ro u s a lg a e th a t , re m a rk a b ly , h a v e th e i r c h lo ro p la s ts lo c a te d w ith in th e lu m e n o f th e ro u g h e n d o p la sm ic re t ic u lu m , n o t in th e cy to so l as in

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th e p la n t k in g d o m ). T h a t p a p e r a lso m a d e m a jo r c h a n g e s in th e c irc u m sc r ip tio n o f th e ex is tin g b o ta n ic a l k in g d o m s F u n g i a n d P la n ta e . T h e six- k in g d o m system o f C a v a lie r -S m ith ( 1981 ö) w as la te r slig h tly m o d ified (C a v a lie r -S m ith , 1 9 83a) b y u s in g th e o ld e r a n d m o re w id e ly fa m il ia r n a m e P ro to z o a , r a th e r th a n P ro tis ta , fo r th e b a sa l e u k a ry o tic k in g d o m [ in e ffec t, b ro a d e n in g th e k in g d o m P ro to zo a o f C a v a lie r -S m ith (1 9 8 1 a )] a n d c re a t in g a n ew p ro to z o a n su b k in g d o m , A rc h e z o a , fo r p u ta t iv e ly p rim itiv e ly a m ito c h o n d r ia l p ro to z o a . S in ce th e n th e b o u n d a r ie s o f th e k in g d o m P ro to z o a h a v e n o t b een to ta lly s ta b le : th e tax o n A rc h e z o a w as la te r(C a v a lie r -S m ith , 1987a) m o d ified b y ex c lu s io n o f th e P a ra b a s a la ( i r ic h o m o n a d s a n d h y p e rm a s tig o te flag e lla te s) , a n d th e rev ised A rc h e z o a w e re seg re g a te d from P ro to z o a as a s e p a ra te k in g d o m . A t th e sam e tim e th e b a c te r ia l o r p ro k a ry o tic ta x a E u - b a c te r ia a n d A rc h a e b a c te r ia , t r e a te d as s u b k in g d o m s b y C a v a lie r -S m ith (1 9 8 1 a , 1 9 8 3 a ), w 'ere ra ised in r a n k to k in g d o m s, th u s c re a t in g a n e ig h t k in g d o m system (C a v a lie r -S m ith , 1987a , 1989a , b), w h ich I su b s e q u e n tly a d v o c a te d (G a v a iie r-S m ith , 1991 a -c , 1993a , 1995a) a n d w h ich h a s b een a d o p te d in c e r ta in g e n e ra l w orks (G o u ld & K e e to n , 1996; M a y n a r d S m ith & S z a th m a ry , 1995).

T h e c e n tr a l p u rp o se o f th e p re s e n t rev iew is to re c o n s id e r th e m e rits o f th e e a r l ie r s ix -k in g d o m system in c o m p a r iso n w ith th e e ig h t-k in g d o m system . A fte r d iscu ssin g th e a d v a n ta g e s a n d d is a d v a n tag es o f e a c h , it w ill b e c o n c lu d e d th a t th e s im p le r s ix -k in g d o m c lassif ica tio n is p re fe ra b le as a g e n e ra l re fe re n c e sy s tem . F in e r p h y lo g e n e tic d is c r im in a tio n ca n b e a c h ie v e d b y m a k in g b e t te r use o f in te r m ed ia te - le v e l c a te g o rie s su ch as su b k in g d o m s a n d in fra k in g d o m s, w 'ith o u t m u ltip ly in g th e n u m b e r o f k in g d o m s. S o m e ch an g es in c irc u m sc r ip tio n o f fo u r o f th e six k in g d o m s a re a lso n e e d e d ; in th e lig h t o f re c e n t m o le c u la r seq u en ce e v id en c e it is n ecessa ry to rem o v e fo u r g ro u p s fro m th e P ro to z o a a n d to p lace th e m in h ig h e r k in g d o m s; th u s M ic ro s p o r id ia a re t r a n s fe r re d to th e F u n g i, M y x o z o a a n d M e so z o a to th e A n im a lia , a n d O p a l in a ta to th e C h ro m is ta . T h is m ak es th e k in g d o m P ro to z o a s u b s ta n tia lly m o re h o m o g en eo u s . T h e p o s tu la te d p h y lo g e n e tic r e la t io n sh ip s b e tw e e n th e k in g d o m s, su b k in g d o m s, a n d th e m o s t d e e p ly d iv e rg e n t in f ra k in g d o m s o f th e p re sen t sy s tem a re sh o w n in F ig . 1.

206 T . C a v a l i e r - S m i t h

ANIMALIAM esozoa

FUNGI CHROMISTA PLANTAE

Cryptista C hrom obio taBilata ria A M yxozoa

E om ycotaR adiata Biliphyta

■►Alveolata

I ch lo rop last hA d in o p o d a S arco m astig o ta^« ^

tu b u la r m itochondria l c ristae sp llceosom al in trons; bikonty

neoka ryotes

p e ro x iso m e s j?A rchezoa PROTOZOA

m itochondria

en d o m e m b ra n e sy s te m , cytoskeleton te trakont cen trio les, nucleus, m itosis, sex

Em pirePROKARYOTA loss of m urein A rchaebacteriaisopreno id

e th e r lipidsP osibacteria

J J o s ^ ^ u te m n e m b r a n ^

Glyco bacteria

I lipopolysaccharideBACTERIA

Lipo bacteria

acyl e s te r m em b ra n e lipids m urein w alls; o u te r m em b ran e

F ig . 1. P o s tu la te d p h y lo g e n e t ic r e la t io n s h ip s b e tw e e n th e six k in g d o m s ( u p p e r c a se ) a n d th e i r su b k in g d o m s . InCra- k in g d o m s a rc a lso sh o w n fo r th e tw o b a sa l p a r a p h y le l ic k in g d o m s , as a r c so m e k ey in n o v a t io n s (w ith in h e a v y b o x es). T h e fo u r m a jo r sy m b io g e n c tic e v e n ts in th e h is to ry o f life a r e sh o w n w ith d a s h e d a r ro w s : (1 ) th e s v m b io g e n e tic o r ig in of m i to c h o n d r ia f ro m a n « - p ro te o b a c ic r iu m , (2 ) th e p r o b a b le o r ig in o f p e ro x iso m e s f ro m a p o s ib a c te r iu m (C a v a l ie r - S m ith , 1 9 9 0 ), (3 ) th e m o n o p h y le t ic o r ig in o f c h lo ro p la s ts f ro m a c y a n o b a c te r iu m , a n d (4 ) th e o r ig in o f th e a n c e s tra l c h ro m is t as a e u k a r y o te - e u k a ry o tc c h im a e r a b e tw e e n a r h o d e l lo p h te r e d a lg a l e n d o s y m b io n t a n d a b id l i a t e d p ro l is l h o s t ; w h e th e r th e h o s t w a s a p ro to z o a n , a s a s su m e d h e re , o r a v e ry e a r ly p la n t is u n c le a r F o r c la r i ty in f ra k in g d o m s a r e n o t sh o w n fo r th e fo u r h ig h e r h o lo p h v le t ic k in g d o m s , A n im a l ia , F u n g i , P la n ta e , a n d C h ro m is ta . T h e d ia g n o s e s o f th e t a x a a r e g iv e n in T a b le 1 a n d th e i r c o m p o s it io n is s u m m a r iz e d in T a b le s 2 - 7 . C h lo ro p la s ts a r c a s su m e d to h a v e o r ig in a te d in th e l a te s t c o m m o n a n c e s to r o f P la n ta e , D is c ic r is ta ta a n d th e a lv e o la te d in o f la g e l la ta p r o to z o a (C a v a lie r - S m ith , 1 9 8 2 ), a n d th e p la s tid s o f e u g lc n o id s a n d a lv c o la te s a r e a s su m e d lo h a v e a r is e n d iv e rg e n t ly f ro m th is p r im a ry e n d o s y m b io s is . H o w e v e r , th e a l te r n a t iv e p o s s ib ility t h a t d in o f la g e l la te s a n d / o r e u g le n o id s o b ta in e d th e i r c h lo ro p la s ts s e c o n d a r ily b y la te r a l t r a n s f e r f ro m a c h ro m o b io te a n d g r e e n a lg a re sp e c tiv e ly , th o u g h c o n s id e re d d is t in c t ly less like ly , c a n n o t c u r r e n t ly b e e x c lu d e d ( C a v a l ie r -S m ith , 1995 a) ; th e so u rc e o f th e n o n -p h o lo s v n th e t ic p la s t id o f c o c c id io m o rp h S p o ro z o a is e q u a l ly u n c e r ta in ( M c F a d d c n & W a lle r , 1 9 9 7 ). F o r s im p lic ity a fifth im p o r ta n t c a s e o f sv m b io g c n e s is is n o t sh o w n : s e c o n d a ry s y m b io g e n c tic la te r a l tr a n s fe r s o f g r e e n a lg a l , p o ss ib ly u lv o p h y tc ( I s h id a el a l., 1 9 9 8 ). c h lo ro p la s ts in to a c c r c o z o a n ( s a r c o m a s t ig o ta h o s t to c r e a te th e a lg a l c la ss C h lo r a r a c h n e a (e .g . Chlorarachnion). T h e leas t c e r ta in f e a tu re s o f th e t r e e a r c th e p o s itio n o f i ts r o o t (so m e a u th o r s f a v o u r a ro o t w ith in th e U n ib a c te r ia r a t h e r th a n th e N e g ib a c te r ia ) a n d o f th e D is c ic r is ta ta (1 8 S r R N A a n d E F I - a ti ces p u t th e m b e lo w th e S a r c o m a s t ig o ta , w h e re a s o th e r p ro te in s p la c e th e m a s sh o w n ).

A revised s ix -k in g d o m system o f life 207

W h e n e s ta b lish in g th e k in g d o m C h ro m is ta (C a v a lie r -S m ith , 1 981a) I m e n tio n e d th a t , a s d is cussed e a r l ie r b y T a y lo r (1978) a n d H ib b e rd (1979), th e re w e re rea so n s fo r th in k in g th a t p ro te ro m o n a d s m a y b e c lo se r to C h ro m o b io ta th a n to P ro to z o a . T h e y h a d som e u l t r a s t r u c tu r a l s im ila ritie s w ith c h ro m is ts a n d so m e w ith th e o p a lin id s , so it a p p e a re d th a t th e y m ig h t b e p h e n o ty p ic a lly in te rm e d ia te b e tw e e n c h ro m is ts a n d p ro to z o a . I n o rd e r to m a k e th e d e f in it io n o f th e C h ro m is ta as s h a rp as possib le , I c o n se rv a tiv e ly k e p t th e p ro te ro m o n a d s in th e k in g d o m P ro to z o a , p la c in g th e m to g e th e r w ith o p a lin id s a n d c y a th o b o d o n id s in th e p ro to z o a n g ro u p P ro te ro z o a , b u t re c o g n iz e d th a t th e b o u n d a ry b e tw e e n c h ro m is ts a n d p ro to z o a n s m ig h t re q u ire s lig h t a d ju s tm e n t in fu tu re . P a tte rs o n (1985) su b se q u e n tly p la c e d p ro te ro m o n a d s a n d o p a lin id s a lo n e to g e th e r in th e o r d e r S lo p a l in id a . L a te r P a tte rso n (1989) a rg u e d th a t s lo p a lin id s sh o u ld b e g ro u p e d w ith h e te ro k o n ts as s tra m e n o p ile s . 1 h a v e since a rg u e d th a t th e g en u s P roteom onas is less closely re la te d to O p a l in id a th a n is th e g en u s Karotomorpha a n d p la c e d th e o rd e rs K a ro to m o rp h id a a n d O p a lin id a to g e th e r in th e class O p a lin e a (C av a lie r- S m ith , 1993a , b) b u t p u t p ro te ro m o n a d s in a s e p a ra te class. A s p a r t o f a r e a p p ra is a l o f th e P ro te ro z o a s t im u la te d b y re c e n t rR N A (r ib o so m a l R N A ) se q u en ces (C a v a lie r -S m ith & C h a o , 1995,1997) I h a v e c re a te d a n e w class P ro te ro m o n a d e a fo r th e P ro te ro m o n a d id a , a b a n d o n e d th e ta x o n P ro te ro z o a a n d g ro u p e d O p a lin e a w ith P ro te ro m o n a d e a in th e s u b p h y lu m O p a l in a ta (C a v a lie r- S m ith , 1 9 9 7 a). I n o rd e r to in c re a se th e h o m o g e n e ity o f th e n ew p ro to z o a n su b k in g d o m N eo zo a a n d th e zo o fla g e lla te p h y lu m N e o m o n a d a , I e x c lu d e d th e rev ised O p a l in a ta from th e m as a p ro tis t ta x o n incertae sed ii. H e re , I a c c e p t th e v iew (P a t te rs o n ,1989) th a t O p a l in a t a (a su b p h y lu m n o w co m p o - s i tio n a lly th e s a m e as th e o rd e r S lo p a lin id a ) a re p ro b a b ly s e c o n d a r ily m o d ified h e te ro k o n ts , a n d th e re fo re p la c e th e m w ith in th e c h ro m is t in f ra - k in g d o m H e te ro k o n ta a n d g ro u p th e m w ith th e h e te ro tro p h ic s u b p h y lu m P seu d o fu n g i (C a v a lie r- S m ith , 1986a , 19896) to fo rm a n ew h e te ro tro p h ic c h ro m is t p h y lu m , B ig y ra , in w h ic h I a lso p la c e th e re c e n tly d isco v e red d is tin c tiv e h e te ro k o n t p ro tis t D evelopayella elegans (T o n g , 1995), fo r w h ich I c re a te a n ew o rd e r , c lass a n d s u b p h y lu m .

I n th e sy s tem o f C a v a lie r -S m ith (1981 a) I re fined th e k in g d o m F u n g i b y re m o v in g o o m y cetes , h y p h o - c h y tr id s , a n d th r a u s to c h y tr id s a n d tra n s fe r r in g th e m in to th e H e te ro k o n ta w ith in th e n ew k in g d o m C h ro m is ta , a n d a rg u in g th a t C h y tr id io m y c e te s , b y

c o n tra s t , sh o u ld b e in c lu d e d in th e k in g d o m F u n g i. T h is c irc u m sc rip tio n o f th e k in g d o m F u n g i (see also C a v a lie r -S m ith , 19876) is n o w a lm o s t u n iv e rsa lly a c c e p te d b y p h y lo g e n e tic a lly o r ie n te d m yco log ists (B runs , W h ite & T a y lo r , 1991), a n d a d o p te d by the a u th o r i ta t iv e D ictionary o f the F ungi (H a w k s w o rth et a l., 1995). I t w ill, th e re fo re , c o m e as a c o n s id e ra b le su rp rise to m yco log ists to le a rn th a t th e k in g d o m F u n g i n o w n eed s to b e d ra s tic a lly e x p a n d e d b y th e a d d it io n o f th e M ic ro sp o r id ia , a p h y lu m o f m in u te in t ra c e l lu la r p a ra s ite s o f a n im a ls . T h o u g h M ic ro sp o r id ia h a v e c h it in o u s sp o res a n d a r e n o t p h ag o - tro p h ic , th e y w e re t r a d it io n a l ly th o u g h t o f as p ro to z o a r a th e r th a n fung i b e c a u se th e i r v eg e ta tiv e cells la c k cell w alls . L ik e O p a l in a ta , th e M ic ro sp o r id ia la c k p e ro x iso m e s ; b u t a s th e y also lack m ito c h o n d r ia th e y w e re p o s tu la te d to b e a rc h e z o a n P ro to z o a (C a v a lie r -S m ith , 1 9 8 3 a ) ; how 'ever, re c e n t p ro te in se q u e n c e d a t a (L i et a l., 1961; E d lin d et al., 1996 ; K e e lin g & D o o little , 1996 ; R o g e r , 1996; G e rm o t e t a l, 1997) s tro n g ly su g g est t h a t th e y a re a c tu a lly h ig h ly d e g e n e ra te fu n g i, w h ic h h a v e seco n d a r i ly lost m ito c h o n d r ia , like th e ru m e n fung i (N eo ca llim as tig a le s ) , w h ic h h a v e a lso b een m ista k e n ly classified as p ro to z o a in th e p a s t. I h e re rem o v e th e M ic ro sp o r id ia fro m th e A rc h e z o a a n d p la c e th e m in s te a d in th e k in g d o m F u n g i, w h e re I g ro u p th e m w ith th e A rc h e m y c o ta in a n ew su b k in g d o m E o m y c o ta . A s th e h ig h e r level classif ic a tio n o f th e k in g d o m F u n g i n e e d s som e rev ision , I d iv id e it in to tw o n e w su b k in g d o m s (E o m y c o ta a n d N e o m y c o ta ) a n d c re a te a few o th e r n ew h ig h level fu n g a l ta x a , a n d a iso v a lid a te som e o f th o se p ro p o sed e a r l ie r (C a v a lie r-S m ith , 19876 ). I p re s e n t a d e ta ile d c lassifica tio n o f th e k in g d o m F u n g i, d o w n to th e level o f subclass.

T h e th iT d re f in e m e n t m a d e h e re to th e c ir c u m sc r ip tio n o f th e P ro to z o a c o m p a re d w ith th e ea r lie r s ix -k in g d o m system (C a v a lie r -S m ith , 1 983a) is th e tra n s fe r o f th e M eso zo a a n d M y x o s p o r id ia in to th e k in g d o m A n im a lia , a s b rie fly in d ic a te d e a r lie r (C a v a lie r -S m ith , 19956 , C a v a lie r -S m ith et al., 1996 a).

T h e reaso n s fo r th e a b o v e c h a n g e s in c ir c u m sc r ip tio n o f th e k in g d o m s P ro to z o a , C h ro m is ta , F u n g i a n d A n im a lia w ill b e e x p la in e d in d e ta i l . I n v iew o f th e n u m e ro u s c h a n g e s in h ig h - le v e l c lassific a tio n o v e r th e p a s t 15 y ea rs , I sh a ll p re se n t a d e ta i le d su m m a ry o f th is rev ised s ix -k in g d o m classif ic a tio n o f th e liv in g w o rld , dow m to th e level o f in f ra p h y lu m .

M y re d e f in itio n o f th e k in g d o m P la n ta e to in c lu d e a ll V ir id a e p la n ta e (g re e n p la n ts ) , G la u c o p h y ta , a n d

208 T . C a v a l i e r - S m i t h

T a b le 1. The revised six-kingdom system o f life

E m p ir e o r S u p e r k in g d o m 1. P R O K A R Y O T A * * D o u g h e r iy 1957 s la t. n o v . A lls o p p 1 9 6 9 ( r ib o s o m e s in th e s a m e c o m p a r tm e n t as th e u su a lly c i r c u la r c h ro m o so m e ) .

K in g d o m B a c t e r ia * * C o h n 1870 s ta t . n o v . C a v a l ie r - S m ith 1983 (sy n . P ro c a ry o ta e M u r r a y 1 9 6 8 : n o in te rn a l c y to s k e le to n , e n d o m e m b r a n c sy s te m , n u c le i , m ito s is o r t r u e sex ).

S u b k in g d o m 1. N e g ib a c tc r ia * C a v a l ie r - S m ith 1987 ( o u te r m e m b r a n e p r e s e n t ; acy l e s te r l ip id s ; w ith sm a ll s ig n a l- r é c o g n i t io n p a r t ic le R N A ) .

In f r a k in g d o m L ip o b a c tc r ia * n e w in f r a k in g d o m (d ia g n o s is : n o l ip o p o ly s a c c h a r id e in o u t e r m e m b r a n e ; m u r c in c e ll w a ll) .

In f r a k in g d o m 2. G ly c o b a c lc r ia * n e w in f ra k in g d o m (d ia g n o s is : l ip o lv s a c c h a r id c in o u te r m e m b r a n e ; ce ll w a l l o f m u r c in o r , r a r e ly , p r o te in ) .

S u b k in g d o m 2 . U n ib a c te r ia * n e w s u b k in g d o m (d ia g n o s is : b a c te r ia w ith n o o u te r m e m b r a n e ; w ith la rg e s ig n a l- r e c o g n i t io n p a r t ic le R N A as in e u k a ry o te s ) .

I n f r a k in g d o m 1. P o s ib a c te r ia * C a v a l ie r -S m ith 1987 s ta t . n o v . (acy l e s te r l ip id s ; o f te n w i th tc ic h o ic a c id s ) .I n f r a k in g d o m 2. A r c h a c b a c tc r ia W o e sc & F o x 1977 s ta t . n o v . ( iso p rc n o id e th e r l ip id s ; m u r e in a b s e n t) .

E m p ir e o r S u p e r k in g d o m 2 . E U K A R Y O T A (c y to sk e le to n , e n d o m e m b r a n c sy s te m , n u c le u s , sex ).

K in g d o m 1. P r o t o z o a * * G o ld fu ss 1818 s ta t. n o v . O w e n 1858 e m . (p h a g o tro p h s p r im it iv e ly w i th o u t p la s tid s , c o lla g e n o r c h i t in o u s v e g e ta t iv e ce ll w a lls ; u n ic e l lu la r , p la s m o d ia l o r c o lo n ia l) .

S u b k in g d o m 1. A r c h e z o a * * C a v a l ie r -S m ith 1983 c m . (k in e tid l e t r a k o n t ; m i to c h o n d r ia a b s e n t ; g e n e s u n s p li t) .S u b k in g d o m 2 . N e o z o a * * C a v a l ie r - S m ith 1993 s ta t . n o v . 1997 (k in e tid ty p ic a lly b ik o n t ; t u b u l a r o r r a r e ly f la t

m i to c h o n d r ia l c r i s i a e ; sp lic c o so m a l in t ro n s c o m m o n ) .In f r a k in g d o m 1. S a r c o m a s t ig o ta * * C a v a l ie r - S m ith 1983 s la t . n o v . e m . (k in e t id b ik o n t o r s e c o n d a r ily u n ik o n t

o r a b s e n t ; m i to c h o n d r ia u s u a l ly w ith t u b u l a r c r is ta e , r a r e ly f la t ( ty p ic a lly n o n -d is c o id ) o r v e s ic u la r ; c o r t ic a l a lv eo li a b s e n t ; p s e u d o p o d ia w h e n p r e s e n t n o n - e ru p i iv c ; a x o p o d ia l m ic ro tu b u le s if p re se n t , n o t s p ira l ly o r h e x a g o n a l ly a r r a n g e d j .

I n f r a k in g d o m 2. D is c ic r is ta ta n e w in f ra k in g d o m (k in e t id l e t r a k o n t o r b ik o n t ; m i to c h o n d r ia o r h y d ro g e n o so m e s p r e s e n t ; c r is ta e d is c o id ; g e n e s m o s tly u n s p l i t ; p s c u d o p o d ia e r u p t iv e w h e n p r e s e n t ; c o r t ic a l a lv e o li a n d a x o p o d ia a b s e n t ) .

I n f r a k in g d o m 3 . A lv e o la ta C a v a l ie r - S m ith 1991 [c o r t ic a l a lv e o li ( r a r e ly s e c o n d a r ily a b s e n t ) ; m i to c h o n d r ia l c r is ta e t u b u l a r o r a m p u ll i fo rm ] .

I n f r a k in g d o m 4 . A c t in o p o d a C a lk in s 1902 s ta t . n o v . C a v a l ie r -S m ith 1996 ( a x o p o d ia w ith h e x a g o n a l o r sp ira l ly a r r a n g e d m ic r o tu b u le s ; c ilia a b s c n l o r fo r d is p e rs a l o n ly ; p o ss ib ly p o ly p h y le tic ) .

K in g d o m 2. A n im a l ia L in n a e u s 1758 e m . C a v a l ie r - S m ith 1995 (u n n e c e s sa ry sy n o n y m M e ta z o a H a e c k e l 1874) ( a n c e s tr a l ly p h a g o t r o p h ic m u lt ic e l is w i th c o lla g e n o u s c o n n e c t iv e tissu e b e tw e e n tw o d is s im ila r e p i th c l ia ) .

S u b k in g d o m 1. R a d ia t a * * L in n a e u s 1758 s ta l . n o v . e m . C a v a l ie r -S m ith 1983 (m u lt ic e l lu la r a n im a ls w ith r a d ia l o r b i r a d ia l s y m m e tr y ; n o a n u s ) .

I n f r a k in g d o m 1. S p o n g ia r ia * D e B la in v ille 1816 (c h o a n o c y te s l in e b o d y c a v i ty ; n e rv o u s sy s te m p r im itiv e ly a b s e n t : sp o n g e s ) .

I n f r a k in g d o m 2. C o e le n te r a ta * L c u c k a r l 1847 c m . a u c l . ( n e rv e n e t) .I n f r a k in g d o m 3. P la c o z o a in f ra k in g . n o v . (w i th o u t b o d y c a v i ty , g u t o r n e rv o u s sy s te m ).

S u b k in g d o m 2. M y x o z o a G ra s s é 1970 s ta t . n o v . ( s e c o n d a r i ly u n ic e l lu la r p a r a s i te s o f b i la te r a l a n im a ls ; sp o res m u l t i c e l lu la r ; c ilia a b s e n t : m y x o sp o r id ia ) .

S u b k in g d o m 3 . B i la te r ia H a ts c h c k 1888 s ta t . n o v . C a v a l ie r - S m ith 1983 ( b i la te ra l , p r im it iv e ly w ith a n u s ) .B ra n c h 1. P ro to s to m ia * G r o b b e n 1908 (b la s to p o re b e c o m e s m o u th ) .

In f r a k in g d o m 1. L o p h o z o a * new ' in f ra k in g d o m (p r im it iv e ly sessile w ith U - s h a p e d g u i a n d c i l ia te d o ra l te n ta c le s w i th c o e lo m ic e x te n s io n s ; e a r ly c i l ia te d l a r v a e tr o c h o p h o rc s , l a t e r o f te n b iv a lv c d ) .

In f r a k in g d o m 2 . C h a e to g n a th i L e u c k a r t 1854 s ta l . n o v . ( n o n -c i l ia tc d ; th in c u tic le n o t m o u l te d ; e m b ry o n ic c n te ro c o e l a b s e n t in a d u l t ) .

I n f r a k in g d o m 3. E c d y s o z o a n e w in f ra k in g d o m ( n o n - c i l i a te d ; th ic k c u tic le t h a t is m o u l te d ; h a c m o c o e l o r p se u d o c o e l) .

I n f r a k in g d o m 4. P la ly z o a n e w in f ra k in g d o m ( s e c o n d a r i ly a c o e lo m a te w o rm s w i th o u t v a s c u la r sy s te m ; a n c e s tra l ly c i l ia te d ) .

B r a n c h 2 . D e u te r o s to m ia G r o b b e n 1908 (b la s to p o re b e c o m e s a n u s ) .I n f r a k in g d o m I . C o e lo m o p o r a s ta t . n o v . ( t r im e r ic c o e lo m , a n te r io r c o m p a r tm e n t w ith e x te r n a l p o re ;

e n te ro c o c lo u s ; c i l ia te d p e la g ic la r v a e ; n e rv e n e t) .

A re v is e d s i x - k in g d o m s y s te m o f l i f e

T a b l e 1- (c o n t.)

209

I n f r a k in g d o m 2. C h o r d o m a H a e c k e l 1874 e m . H a ts c h c k 1888 (se h iz o c o c lo u s o r c o e lo m a b s e n t ; la rv a e ta d p o le - l ik e ; h o llo w d o r s a l n e rv e c o rd ) .

S u b k in g d o m 4 . M e s o z o a V a n B e n e d e n 1877 s ta t . n o v . ( c i l ia te d m u lt ic e i lu la r p a r a s i t e s ; n o n e rv o u s sy s te m o r g u i) .

K in g d o m 3. F u n g i L in n a e u s 1753 s la t . n o v . N c e s 1817 e m . (v e g e ta t iv e a n d / o r sp o re c e ll w a lls o f c h i t i n a n d ß - g lu c a n ; n o p h a g o c y to s is ) .

S u b k in g d o m 1. E o m y c o ta * * s u b k in g . n o v . (d ia g n o s is : h y p h a c w i th o u t p e r fo r a te s e p ta ; w i th o u t d ik a r y o t ic p h a s e : c c llu la e n o n b in u c l c a t a e ; s e p ta u s i la ic a b s e n s ; si p ra e s e n s n o n p e r fo r a ta ) .

S u b k in g d o m 2. N c o m y c o la s u b k in g . n o v . (d ia g n o s is : u s u a l ly w ith a d ik a ry o t ic p h a s e ; h y p h a e , i f p r e s e n t , w ith p e r fo r a te s e p ta : c e l lu la c b in u c l e a t a ? p lc r u m q u c p r a c s c n te s ; e n d o s p o ra a u t a s c o sp o ra a u t b a s id io s p o r a in s t r u c ta ) .

K in g d o m 4 . P la n ta e H a e c k e l 1866 e m . C a v a l ie r - S m ith 1981 (p la s t id s w ith d o u b le e n v e lo p e in c y to s o l; s t a r c h ; n o p h a g o c y to s is ) .

S u b k in g d o m 1. B i l ip h y ta * C a v a l ie r - S m ith 1981 (p h y e o b il is o m e s ; s in g le th y la k o id s ; s t a r c h i n c y to s o l) .I n f r a k in g d o m 1. G la u c o p h y ta in f ra k in g . n o v . ( d ia g n o s is : p c p t id o g ly c a n in p la s l id e n v e lo p e : p la s t id a c

p c p t id o g ly c a n u m in s t r u c ta e ) .I n f r a k in g d o m 2. R h o d o p h y ta in f ra k in g . n o v . (s in e p e p l id o g ly c a n o : p la s tid e n v e lo p e la c k s p c p t id o g ly c a n ) .

S u b k in g d o m 2. V i r id a e p la n ta e C a v a l ie r - S m ith 1981 ( c h lo ro p h y ll a a n d b ; th y la k o id s s l a c k e d ; s ta rc h in p la s tid s t r o m a ; c i l ia ry t r a n s i t io n n in e - fo ld s t a r : g r e e n p la n ts ) .

I n f r a k in g d o m 1. C h lo r o p h y ta C a v a l ie r - S m ith 1993 (g re e n a lg a e ) .I n f r a k in g d o m 2 . C o r m o p h y ta E n d lic h e r 1836 s ta t . n o v . ( e m b ry o p h y te s ) .

K in g d o m 5 . C h r o m is t a C a v a l ie r - S m ith 1981 e m . ( c h lo ro p la s ts w ith c h lo ro p h y l l c in s id e a p e r ip la s t id m e m b r a n e w ith in th e ro u g h e n d o p la s m ic r e t ic u lu m lu m e n a n d / o r w ith r ig id b ip a r t i t e o r t r ip a r t i t e c i l ia ry h a ir s ) .

S u b k in g d o m 1. C r y p t i s t a C a v a l ie r - S m ith 1989 (e je c tiso m e s ; u su a lly w ith b ip a r t i t e h a i r s o n b o th c ilia , t iu e le o m o rp h a n d p h y c o h i l in s ; c r is ta e f la t te n e d tu b u le s ; p e l l ic u la r p la te s ) .

S u b k in g d o m 2. C h r o m o b io ta C a v a l ie r -S m ith 1991 (c r is ta e t u b u l a r ; p o s te r io r c i l iu m o f te n a u to f lu o re s c e n t ; no n u c le o m o r p h , e je c tiso m e s , p e l l ic u la r p la te s o r p h y c o b il in s ) .

I n f r a k in g d o m 1. H e te r o k o n ta C a v a l ie r - S m ith 1986 s ta t . n o v . 1995. e m . ( r ig id t r ip a r t i t e o r b ip a r t i t e h a ir s on a n t e r io r c i l iu m o n ly o r , r a r e ly , o n cell b o d y ; n o h a p lo n e m a ) .

I n f r a k in g d o m 2. H a p to p h y ta C a v a l ie r - S m ith 1995 ( h a p to n e m a ; h a ir s u n ip a r t i t c tu b u le s , k n o b h a ir s o r a b s e n t) .

* P ro b a b ly p a r a p h y le t i c ta x o n .* * A lm o s t c e r ta in ly p a r a p h y le t ic .T h e c la s s if ic a tio n o f e a c h o f th e k in g d o m s is g iv e n in m o re d e ta i l in T a b le s 2 - 7 , w ith e x a m p le s o f re p re s e n ta t iv e s

o f th e m a jo r ta x a . I t is d o u b t f u l i f th e m o d if ic a tio n o f th e sp e llin g o f th e n a m e A r c h a e b a c te r ia in Bergey ¡ M a n u a l to Archaeobacleria ( G ib b o n s & M u r r a y , 1978) w as c o r r e c t ; i f a r c h a e - w as d e r iv e d f ro m th e G re e k archaias ( a n c ie n t) th e n i t is a s te m a n d th e ‘ o ’ sh o u ld b e in s e r te d a c c o r d in g to th e ru le s o f th e b o ta n ic a l c o d e b u t th is is n o t r e q u i re d by th e b a c te r io lo g ic a l c o d e ; b u t i f i t w a s d e r iv e d f ro m th e G re e k arche (b e g in n in g ) , A r c h a e b a c te r ia is a c o r re c tly fo rm e d p s e u d o c o m p o u n d w o rd In w h ic h archae r e ta in s th e c a se e n d in g -ae, a n d as archae is a w h o le w o rd (n o t th e s te m arch-) i t w o u ld b e in c o r r e c t lo in se r t th e ‘ o ’. F o r s ta b il i ty , I p re fe r lo k e e p th e o r ig in a l s p e llin g a n d to a ssu m e t h a t W o e se & F o x (1 9 7 7 a ) m a d e n o e r ro r . T h e m o re r e c e n t c h a n g e to A r c h a e a (W o e se , K a n d i e r & VVhcclis, 1990) is b o th to ta l ly u n n e c e s s a ry a n d h ig h ly u n d e s i r a b le ; i ts u se s h o u ld b e m o s t s tro n g ly d is c o u ra g e d ( C a v a l ie r -S m ith , 1 9 9 2 6 ) .

R h o d o p h y t a , a n d th e s e t h r e e g r o u p s a l o n e ( C a v a - l i e r - S m i t h , 1 9 8 1 a ) , is n o t y e t w i d e l y a c c e p t e d , l a r g e l y b e c a u s e o f a f o r m e r l y w i d e s p r e a d b e l i e f i n t h e p o l y p h y l e t i c s y m b i o t i c o r i g in s o f c h l o r o p l a s t s

( M e r e s c h k o w s k y , 1 9 1 0 ; M a r g u l i s , 1 9 7 0 , 1 9 8 1 ; R a v e n , 1 9 7 0 ) . B u t a s t h e t h e o r y o f t h e m o n o p h y l e t i c s y m b i o g e n e t i c o r i g i n o f c h l o r o p l a s t s ( C a v a l i e r -

S m i t h . 1 9 8 2 ) , u p o n w h i c h m y c i r c u m s c r i p t i o n o f P l a n t a e w a s b a s e d , is i n c r e a s i n g l y w i d e l y a c c e p t e d ( B h a t t a c h a r y a & M e d l i n , 1 9 9 5 ) , a n d a s i t l o g i c a l l y

f o l lo w s t h a t t h e t h r e e m a j o r p l a n t g r o u p s a r e d e r i v e d

f r o m a s in g le p h o t o s y n t h e t i c c o m m o n a n c e s t o r , I t h i n k t h a t i t w i l l b e o n l y a m a t t e r o f t i m e b e f o r e t h e l o g i c o f a c c e p t i n g t h e m o n o p h y l y o f t h e k i n g d o m

P l a n t a e sensu C a v a l i e r - S m i t h ( 1 9 8 1 a ) w il l a l s o b e

g e n e r a l l y r e c o g n i z e d , a s i t a l r e a d y h a s b e e n b y R a g a n & O u t t e l l ( 1 9 9 5 ) . I h a v e t h e r e f o r e s e e n n o r e a s o n to m o d i f y t h e c i r c u m s c r i p t i o n o f t h e k in g d o m P l a n t a e o r i t s s u b d i v i s i o n i n t o t w o s u b k i n g d o m s ( V i r i d a e p l a n t a e a n d B i l i p h y t a ) s i n c e C a v a l i e r - S m i t h

( 1 9 8 1 a ) , a n d e x p e c t t h e k i n g d o m t o c o n t i n u e t o b e s t a b l e i n t h e f u t u r e .

2 1 0 T . C a v a l i e r - S m i th

A n o v e rv iew o f th e rev ised s ix -k in g d o m system is g iv e n in T a b le 1, w h ic h in c lu d e s a ll th e s u p ra p h y le t ic ta x a , w ith d ia g n o se s sh o w in g h o w th e y m a y be d is tin g u ish e d . I n o id e r to sav e sp a c e in th e la te r ta b le s d e a lin g w ith th e p h y la , s u b p h y la a n d in fra - p h y la o f e a c h k in g d o m d iag n o se s a r e g iv en o n ly for n e w o r s u b s ta n tia lly e m e n d e d ta x a . D e sp ite th e c re a t io n h e re o f five n ew p h y la , I a c c e p t o n ly 60 p h y la fo r th e e n t i r e liv in g w o rld , m a n y few er th a n th e 92 re c o g n iz e d by M a rg u lis a n d S c h w a rtz (1988) o r th e 100 u sed by M ö h n (1984 ). I a m n o t a c tu a lly a ‘ b o rn s p l i t t e r ’ (C o rliss , 1994). V iru se s a re best th o u g h t o f a s la te ra l ly tra n sm iss ib le p a ra s it ic g en e tic e le m e n ts , n o t as liv in g o rg an ism s , so I d o n o t a t te m p t to classify th e se im p o r ta n t b io lo g ica l e n ti tie s h e re .

II. P H IL O S O P H IC P R E L IM IN A R IE S

(1) D a r w in ia n e v o lu t io n a r y c la s s if ic a t io n c o n tr a s te d w ith H e n n ig ia n c la d if ic a t io n

E v e r s ince D a rw in , i t h a s b e e n a c c e p te d t h a t ‘ th e sy s te m a d s t is p r im a r i ly a m o rp h o lo g is t w h o se ta sk is to d is c o v e r th e tru e p h y lo g e n e tic r e la tio n s h ip s ’ as C u m m in g s (1 9 1 6 : 254) n o te d 80 y ea rs ag o . D a rw in ia n e v o lu t io n a ry c lassifica tio n s ta k e in to a c c o u n t b o th th e b r a n c h in g p a t te rn s a n d th e d e g re e o f c h a n g e a lo n g d if fe re n t b ra n c h e s , a n d a r e th e re fo re tru ly p h y lo g e n e tic (M a y r & A sh lock , 1991) r a th e r th a n p u re ly c la d is tic o r p u re ly p h e n e tic . A b a la n c e d c la ss if ica tio n a im s to su b d iv id e a ta x o n like E u k a ry - o ta in to a n u m b e r o f s u b o rd in a te ta x a o f lo w e r r a n k in su ch a w a y a s to m a x im iz e th e d e g re e o f s im ila r i ty w ith in e a c h ta x o n , w h ile e n su r in g th a t n o n e o f th e m is p o iy p h y le tic . S in ce o rg an ism s c a n v a ry in m a n y d if fe re n t c h a ra c te rs , a n d in w ays v a ry in g fro m th e tr iv ia l to th e p ro fo u n d , it is e ssen tia l to w e ig h th e i r re la tiv e im p o r ta n c e . L a m a rc k (1810) in i t ia te d th e id e a o f g en e a lo g ic a l c la ssif ica tio n , b u t i t w as D a rw in (1 8 5 9 ), H a e c k e l (1866 , 1868) a n d L a n k e s te r (1877) w h o first re a lly p o p u la r iz e d th e n o tio n o f p h y lo g e n e tic c la s s ic a tio n a s th e c e n tr a l g o a l o fsy s te m a tic s . H aeck e l (1866) in t ro d u c e d th e te rm s p h y lo g e n y , p h y lu m , m o n o p h y le tic a n d c lad u s , w h ils t L a n k e s te r (1977) g a v e us th e c o n c e p t o f a g r a d e a n d e n c o u ra g e d th e E n g lish -sp e a k in g w o rld to su b s titu te H a e c k e l’s te rm p h y lu m fo r su b k in g d o m . T h e s e e a rly p io n e e rs o f p h y lo g e n e tic c la ss if ica tio n u sed b o th g ra d e s a n d c la d e s as ta x a in th e i r in f lu e n tia l c lassifica tions.

W h e n I first a rg u e d th a t th e k in g d o m s o f life n e e d e d rec la ss ify in g o n p h y lo g e n e tic p rin c ip le s to m a k e th e m m o n o p h y le tic (C a v a lie r -S m ith , 1978), I

w as c o m p lim e n te d b y c e r ta in c lad is ts w h o m ista k e n ly th o u g h t I w as a p p ly in g th e p rin c ip le s o f H e n n ig (1966) b ecau se I w as u s in g c la d is tic re a so n in g a n d a d v o c a t in g a p h y lo g e n e tic c lassifica tion w ith s tr ic tly m o n o p h y le tic ta x a . H o w e v e r, I h a d n o t th e n ev en h e a rd o f H e n n ig o r h is c o n fu s in g red e f in itio n o f th e te rm m o n o p h y le tic , w h ic h I d o n o t a c c e p t. L ik e classica l p h y lo g e n e tic is ts , I use th e w o rd m o n o p h y le tic to in c lu d e b o th h o lo p h y le tic (A shlock , 1971, i.e . m o n o p h y le tic sensu H e n n ig , 1966) a n d p a ra p h y le tic . I d o , h o w ev e r, a c c e p t H e n n ig ’s re d e f in it io n o fH u x le y 's (1 957 , 1959) te rm c la d e , w h ic h w as o rig in a lly d e fin e d u s in g th e c lassica l, n o t th e H e n n ig ia n d e f in it io n o f m o n o p h y ly . (T h e e a r l ie r use o f th e w o rd c la d e in b io lo g y b y L a n k e s te r (1 9 1 1 : 1031) as a n a n g lic iz a tio n fo r H a e c k e l’s (1868) ta x o n o m ic c a te g o ry o f c la d u s , e q u iv a le n t in ra n k to in f ra p h y lu m in th e p re s e n t sy s tem , is n o lo n g e r c u r r e n t : th e R e n a is s a n c e u sa g e o f ‘c la d e ’ to d e n o te a p la g u e o r d is a s te r is e v e n m o re o b so le te .) H e n n ig a n d h is fo llow ers h a v e d o n e m u c h to in c rea se th e r ig o u r o f p h y lo g e n e tic a n a ly s is , b u t th is a d v a n c e h a s b e e n b ro u g h t a t th e co st o f som e v e rb a l con fus ion a n d m u c h h a rm fu l d o g m a tis m . F u r th e rm o re , th o u g h c la d is tic an a ly s is is s im p ly fo rm a lized p h y lo g e n e tic c o m m o n sense, a n d sh o u ld b e s tro n g ly e n c o u ra g e d , H e n n ig ia n ta x o n o m y h a s tw o g ra v e defec ts, one p ra c t ic a l a n d o n e th e o re tic a l.

P ra c tic a lly , i t le a d s to se rious in s ta b ili tie s in c lassif ica tio n a n d n o m e n c la tu re . T h e g re a t p ra c t ic a l m e r it o f a D a rw in ia n e v o lu t io n a ry c la ss if ica tio n is th a t it sh o u ld b e m u c h m o re s ta b le , since w h e th e r a ta x o n is h o lo p h y le tic o r p a ra p h y le tic is ir re le v a n t to its c lassif ica to ry ro le . T h e r e a re m a n y th o u sa n d s o f ta x a w h e re w e d o n o t k n o w w h e th e r th e y a re p a ra p h y le tic o r h o lo p h y le tic . A c c o rd in g to H e n n ig ia n p rin c ip le s , w h e n e v e r a n y ta x a b ecom e c lea rly e s ta b lish e d as p a ra p h y le t ic w e w o u ld h a v e to sp lit th e m u p , a b a n d o n th e i r n a m e s a n d in v e n t tw o o r m o re n e w ta x a . T h is w o u ld b e especia lly n o m e n c la tu ra lly d e s ta b il iz in g fo r g e n e ra , a la rg e p ro p o r tio n o f w h ic h m a y b e p a ra p h y le tic .

T h e o re tic a lly , th e H e n n ig ia n a t te m p t to re s tr ic t ta x a to c lad es, a n d fo rb id p a ra p h y le tic g ro u p s is in c o m p a tib le w ith th e b asic p u rp o se o f p h y lo g e n e tic c la ssif ica tio n , ev en th o u g h it m is le a d in g ly m a s q u e ra d e s u n d e r th a t n a m e . W h a t a b io lo g ica l c lassif ica tio n a im s to d o is to a r r a n g e o rg an ism s in a h ie ra rc h ic a l series o f n e s te d ta x a , in w h ich each m o re -in c lu s iv e h ig h e r-le v e l ta x o n is su b d iv id e d c o m p reh en s iv e ly in to less-inc lu sive ta x a a t th e n e x t level below '. T h e re a r e tw o key w o rd s h e re : h ie ra rc h ic a l a n d co m p reh en siv e . A set o f n e s te d c lad e s is

A revised s ix -k in g d o m system o f life 211

Cladification C lassification

C lade E C lade D

C lade A C lade B

C lade C

Taxon E Taxon D

Taxon F* Taxon A Taxon B

Taxon H* Taxon G* Taxon C

F ig . 2 . C o n t r a s t b e tw e e n (a) c la d if ic a t io n a n d (b) c la s s if ic a tio n . F ro m th e s a m e p h y lo g e n e t ic t r e e w ith h o lo p h y le t ic r e c e n t sp e c ie s 1 lo 6 a n d p a r a p h y le t i c a n c e s tra l sp e c ie s 7 to 15 o n e c a n p r o d u c e e i th e r a lis t o f n e s te d c la d e s o r a c o m p re h e n s iv e c la s s if ic a tio n . I n th e c la s s if ic a tio n t a x o n D is c o m p re h e n s iv e ly s u b d iv id e d in to th r e e t a x a o f lo w e r a n d e q u a l r a n k (A , B , F ) ; A a n d B a r e h o lo p h y le t ic a n d F is p a r a p h y le t i c . I n th e c la d if ic a t io n , c la d e D is s u b d iv id e d in to tw o c la d e s A a n d B w ith th e s a m e c o m p o s it io n a s th e h o lo p h y le tic l a x a A a n d B p lu s a r e s id u e in c lu d in g sp ec ies 10 lo 12 w h ic h is n o t p la c e d in a n y s u b g r o u p o f c la d e D . T h e c la d if ic a t io n is n o t a c o m p re h e n s iv e c la s s if ic a tio n o f c la d e D , b e c a u s e th is p a r a p h y le t i c re s id u e c o m p r is in g sp e c ie s 10 to 12 is n o t l is te d u n d e r c la d e D e v e n th o u g h i t is p a r t o f t h a t c la d c . T h e size o f th is p a r a p h y le t i c re s id u e c o u ld b e re d u c e d in a n a l te r n a t iv e c la d if ic a t io n b y m o v in g th e b o u n d a r ie s o f c la d e s A a n d B f ro m j u s t b e lo w sp ec ies 7 a n d 8 to ju s t a b o v e sp ec ies 1 2 ; b u t a s sp e c ie s 12 is a n c e s tra l to b o th c la d o s A a n d B , i t c a n n o t b e in c lu d e d in e i th e r . N o c la d e c a n b e c o m p re h e n s iv e ly s u b d iv id e d in to s u b d a d e s . A c la d i f ic a t io n c a n n e v e r b e a c o m p re h e n s iv e c la s s if ic a t io n s in c e i t o m its t h e p a r a p h y le t i c r e s id u e s w h ic h a c o m p re h e n s iv e c la s s if ic a t io n m u s t in c lu d e ( t a x a F . G a n d H in th is e a se ) . T h e c la d if ic a t io n o n th e le f t is c o n g r u e n t w ith th e c la s s if ic a tio n o n th e r ig h t . W h e n c o m p re h e n s iv e ly s u b d iv id e d in to ta x a o f e q u a l r a n k , it is lo g ic a lly in e s c a p a b le t h a t e v e ry m o n o p h y le t ic t a x o n (w h e th e r h o lo p h y le t ic o r p a r a p h y le t ic ) m u s t in c lu d e a t le a s t o n e p a r a p h y le t i c ta x o n . A c la d if ic a t io n is a m o s t u se fu l s te p to w a rd s a p h y lo g e n e t ic c la s s if ic a tio n b u t it d o e s n o t c o n s t i tu te o n e in its o w n r ig h t. I f p a r a p h y le t i c t a x a a r e e x p lic i t ly id e n t i f ie d in a p h y lo g e n e t ic c la s s if ic a tio n o n e c a n r e c o n s t r u c t th e c la d if ic a t io n o n w h ic h i t is b a s e d b y d e le t in g th e m . B u t o n e c a n n o t m o v e f ro m a p h y lo g e n e tic tre e to a c la s s if ic a tio n w i th o u t e x e rc is in g ta x o n o m ic ju d g e m e n t , w h ic h is n e c e s sa ry b o th in d e c id in g w h ic h c la d o s sh o u ld b e t r e a te d as t a x a a n d w h e th e r th e p a r a p h y le t i c r e s id u e sh o u ld b e t r e a te d as a s in g le t a x o n o r s u b d iv id e d . J u d g e m e n t is lik ew ise n e e d e d a b o u t th e a p p r o p r i a t e r a n k fo r e a c h ta x o n .

h ie ra rc h ic a l , b u t b e cau se it is n o t c o m p re h e n s iv e a t e ach level in th e h ie ra rc h y , i t is m u c h to o in c o m p le te to b e p ro p e r ly c a lled a c lassifica tion . E rn s t M a y r ip e rs . c o m m .) h a s re c e n tly ca lled su ch a se t o f n e s te d c lad e s a c la d if ic a tio n . F ig u re 2 c o n tra s ts th e w a y in w h ic h a D a rw in ia n e v o lu t io n a ry c lassif ica tio n s u b d iv id e s a p h y lo g e n e tic tre e to p ro d u c e a c o m p re h e n s iv e c la ss if ica tio n o f th e o rg an ism s m a k in g u p th e tre e , w h e re a s H e n n ig ia n c la d if ic a tio n o f th e sam e o rg a n ism s y ields a n in c o m p le te su b d iv is io n o f h ig h e r -

level g ro u p s . C la d is ts h a v e lo n g a c c e p te d th a t th e in a b ili ty to classify a n c e s tra l a n d m a n y fossil ta x a is th e A ch illes hee l o f H e n n ig ia n c la ss if ica to ry p r in cip les, a n d re fe r to i t as a p ro b le m ; i t is n o t a p ro b le m a t a ll fo r sy s tem atic s , b u t m e re ly a basic d e fec t in th e H e n n ig ia n ideas o n c lassifica tion . O b v io u s ly , i f you asse rt th a t y o u m u s t n o t m ake p a ra p h y le tic g ro u p s th e n y o u c a n n o t p ro p e r ly classify a n c e s tra l species ex c lu d e d fro m a p a r t ic u la r c la d e . N o c o m p re h e n s iv e p h y lo g e n e tic c lassif ica tion

212 T . C a v a l i e r - S m i t h

is e v e n th e o re tic a lly poss ib le un less o n e accep ts p a ra p h y le t ic as w ell h o lo p h y le tic la x a . T h e d o g m a a g a in s t p a r a p h y le t ic ta x a is lo g ica lly in c o m p a tib le w ith th e a c c e p ta n c e o f b o th e v o lu tio n b y d e scen t a n d th e g o a l o f ta x o n o m y as th e c re a t io n o f a co m p re h e n s iv e p h y lo g e n e tic c lassif ica tio n o f all o rg a n ism s , b o th e x ta n t a n d e x tin c t.

A s i t is th e o re tic a lly u n so u n d , a n d in p ra c t ic e in c re a se s n o m e n c la tu ra l a n d c la ss if ica to ry in s ta b i lity , th e d o g m a a g a in s t p a ra p h y le tic g ro u p s h a s b een m o s t d e t r im e n ta l to sy s tem atic s . C lad is ts , r ig h tly im m e n se ly im p re ssed w ith th e lo g ic a n d g re a t v a lu e o f H e n n ig ia n p r in c ip le s fo r p h y lo g e n e tic s , h a v e n a tu r a l ly b e e n r e lu c ta n t to a c c e p t th a t th e y c a n be so fa ta lly f law ed w h e n a p p lie d to ta x o n o m y . S o m e d o reco g n ize th is c e n tr a l flaw , b u t say th a t in p ra c t ic e m o s t ta x o n o m is ts d e a l o n ly w i th e x ta n t o rg a n ism s o r t h a t it is n e v e r poss ib le to reco g n ize a n c e s to rs w ith c e r ta in ty . H o w e v e r, w e so m etim es c a n re c o g n iz e a n c e s to rs a n d n e e d to c lassify th em . F u r th e rm o re , n o t a l l a n c e s to rs a re e x tin c t. I n p la n ts , n e w a llo p o ly p lo id spec ies a r e c re a te d b y h y b r id iz a t io n b e tw e e n tw o a n c e s tra l spec ies fo llow ed by p o ly p lo id iz a tio n . I n se v e ra l in s ta n c e s , b o th a n c e s tra l species h a v e b een u n a m b ig u o u s ly id e n tif ie d a n d b o th a r e e x ta n t . A w ell k n o w n e x a m p le is th e fo rm a tio n o f th e n ew g rass Spartina anglica b y a llo p o ly p lo id y fro m th e a n c e s to rs S . alterniflora a n d S. m aritim a . T h e tw o a n c e s to rs a re b o th p e rfec tly g o o d p a ra p h y le t ic ta x a , a n d as b io lo g ica l spec ies a re n a tu r a l ta x a , d is t in c t fro m e a c h o th e r a n d fro m th e ir d e s c e n d a n t spec ies S . anglica. P a ra p h y le tic species a rc th e re fo re as n a tu r a l as h o lo p h y le tic ones. A p a r t fro m th e sp e c ia l case o f b io lo g ica l species, p a r a p h y le tic a n d h o lo p h y le tic ta x a a re b o th p a r t ly a r tif ic ia l c o n s tru c ts o f ta x o n o m is ts (w h e th e r th e y a r e a sex u a l species o r ta x a o f h ig h e r ra n k ) . F ro m su ch a p e rsp e c tiv e a h o lo p h y le tic ta x o n is n o t c re a te d by th e o rig in o f a n e w s y n a p o m o rp h y , b u t b y th e d ec is io n o f a sy s te m a tis t to su b d iv id e a n h is to rica lly c o n tin u o u s p h y lo g e n e tic t r e e a t t h a t p o in t . A s I h a v e stressed p re v io u s ly (C a v a lie r -S m ith , 1 9 9 3 a ), ev e ry such c u t t in g o f f o f a h o lo p h y le tic b r a n c h n ecessa rily s im u lta n e o u s ly g e n e ra te s a p a ra p h y le tic stem . I f I c u t a tre e in to p ieces, e a c h p iece , w h e th e r i t is a te r m in a l p ie c e w ith o n e c m o r a s te m p ie c e w ith tw o o r m o re , is b o th a r t if ic ia l a n d n a tu r a l . E a c h c o n tin u o u s se g m e n t ow es its c o n tin u ity to n a tu r a l p rocesses, w h e re a s its s e p a ra tio n fro m o th e rs is th e re su lt o f h u m a n , i.e . a r t if ic ia l in te rv e n tio n . I f I g ro u p to g e th e r c u t p ieces th a t w ere n e v e r jo in e d o n th e tree , su ch jo in in g w o u ld b e to ta lly u n n a tu r a l , w h ich is w h y p o ly p h y le tic g ro u p in g h as lo n g b e e n a c c e p te d

as m u c h m o re a r tif ic ia l th a n a m o n o p h y le tic g ro u p in g . F o r m o n o p h y le tic g ro u p s (w h e th e r p a ra p h y le tic o r h o lo p h y le tic ) , th e ir c o h e re n c e is th e re su lt o f h is to ric a l g e n e tic c o n tin u ity b e tw e e n a ll m e m b e rs o f th e g ro u p : it is th e i r d is c o n tin u ity fro m o th e r g ro u p s th a t is a r t if ic ia l (ex cep t fo r b io lo g ica l species). T h e c la im th a t a c la d o g ra m o r p h e n o g ra m c a n be co n v e rte d in to a c la ss if ica tio n w ith o u t a r tif ic ia l cu ts ac ro ss th e n a tu r a l p h y lo g e n e tic c o n tin u u m (N elson & P la tn ic k , 1981} is a t b e s t a sp u r io u s h a l f t r u th ; c la d o g ra m s a n d p h e n o g ra m s c a n b e c la im e d to b e as d is c o n tin u o u s as c la ss if ica tio n s o n ly b e c a u se th e cu ts ac ro ss th e p h y le tic c o n tin u u m h a v e a lr e a d y been m a d e b y c lassica l ta x o n o m is ts w h e n c re a t in g th e d is c re te ta x a th a t fo rm th e ra w m a te r ia ls fo r c lad is tic a n d p h e n e tic ana ly s is . T h e c la im invo lves a n e le m e n t o f m y o p ic se lf-d e c e p tio n th a t a llow s som e c la d is ts to c la im falsely th a t H e n n ig ia n sy s tem a tic s is m o re n a tu r a l th a n classica l p h y le t ic ta x o n o m y (S tuessy ,1990). N o c la ss if ica tio n c a n b e to ta lly n a tu r a l .

W h e th e r a ta x o n is p a ra p h y le t ic o r n o t is ir re le v a n t to its v a lid ity as a ta x o n . I t is a lso ir re le v a n t to m a n y o f th e uses to w h ic h c lassif ica tions a r e p u t, such a s a r r a n g in g sp ec im en s in a m u seu m , o rg a n is in g th e c h a p te rs in a b io logy te x tb o o k , o r p ro v id in g a c o n v e n ie n t la b e l, e .g . b a c te r ia o r fung i, fo r a g ro u p o f s im ila r o rg a n ism s . B u t th e d is tin c tio n is im p o r ta n t in c e r ta in uses to w h ic h c lassif ica tions a r e so m etim es p u t. T w o c o m m o n ex am p le s a re the ch o ice o f m o d e l system s a n d th e s tu d y o f g ro u p ex tin c tio n .

A b io log is t w ish in g to choose a p ro to z o a n a s a m o d e l system fo r u n d e rs ta n d in g a n im a l ce ll b io logy w o u ld b e q u ite m is ta k e n in su p p o s in g th a t a s all p ro to z o a a r e classified in th e sam e k in g d o m it does n o t m a t te r w h ic h is ch o se n . O b v io u s ly , som e m e m b e rs o f such a p a ra p h y le tic g ro u p a re c la d i- s tica lly m o re c losely re la te d to a d e r iv e d ta x o n th a n o th e r s : fo r e x a m p le , c h o a n o fla g e lla te s w o u ld be m u c h m o re s im ila r to a n im a l cells th a n w o u ld re to r ta m o n a d s . L ikew ise , th e e x tin c tio n o f a ll m e m bers o f a p a ra p h y le t ic g ro u p , in c o n tr a s t to th a t for a h o lo p h y le tic g ro u p , d o es n o t c o n s titu te e x tin c tio n o f th e e n tire lin eag e . B u t th e m is ta k e n a ssu m p tio n th a t it does, like th e a s su m p tio n th a t a ll m e m b e rs o f a g ro u p a r e e q u a lly re la te d to a n o th e r g ro u p , a re m isuses, n o t uses, o f a c la ssif ica tio n . W h e re p rec ise p h y lo g e n e tic re la tio n sh ip s a re im p o r ta n t fo r a sc ien tific p ro b le m , sc ien tis ts sh o u ld base th e ir re a s o n in g d ire c tly o n p h y to g en ie s a n d n o t use classifica tions as a c ru d e s u r ro g a te fo r th e re a l th in g . T h e p u rp o se o f c lassifica tio n is to p ro v id e a sim p lified re fe ren ce system th a t is b io lo g ica lly so u n d a n d w id e ly useful.

A revised s ix -k in g d o m system o f life 213

I t s h o u ld b e c o m p a tib le w ith th e p h y lo g e n y , b u t it c a n n o t se rv e its c e n tr a l s im p lify in g p u rp o s e un less it leaves o u t som e o f th e fine d e ta i l a b o u t re la tio n sh ip s th a t a re e ssen tia l fo r som e p h y lo g e n e tic p u rp o se s . O n e c a n use a p h y lo g e n y as a basis fo r m a k in g a c la s s if ic a tio n , b u t o n e c a n n o t lo g ica lly d e d u c e a fu lly d e ta i le d p h y lo g e n y fro m a c la ss if ica tio n . N o r is a p h y lo g e n y su ffic ien t to g iv e a c la ss if ica tio n . A p h y lo g e n y a n d a c lassif ica tio n m u s t b e c o n g ru e n t (i.e. n o t c o n tr a d ic to ry ) b u t th e y a r c d if fe re n t w ays o f a b s t ra c t in g fro m a n d re p re se n tin g b io lo g ic a l r e la t io n sh ip s. I t is h ig h ly d e s ira b le th a t ta x o n o m is ts p u b lish a n e x p lic it p h y lo g e n y a n d s ta te m e n t o f th e i r p h y lo g e n e tic a ssu m p tio n s a t th e sam e tim e as th e ir c la s s if ic a tio n , a p ra c t ic e I h a v e lo n g fo llow ed (C a v a lie r -S m ith , 1978). T h is w ill a llo w users to use w h ic h e v e r is m o s t a p p ro p r ia te to th e i r needs. I n o rd e r to a le r t u sers o f c la ssif ica tio n s to th e som etim es im p o r ta n t d iffe ren ces b e tw e e n h o lo p h y le tic a n d p a ra p h y le t ic ta x a it w o u ld b e go o d p ra c t ic e if, w h e re k n o w n , these a r e c le a r ly d is tin g u ish e d . I n T a b le s 1 -7 in th is rev iew I m a rk th o se ta x a th a t a re a lm o s t ceT ta in ly p a ra p h y le t ic a n d th o se w h ic h , in m y p h y lo g e n e tic ju d g e m e n t, a re p ro b a b ly p a ra p h y le tic . T a x a n o t so id e n tif ie d in c lu d e n o t o n ly th o se k n o w n o r th o u g h t to b e h o lo p h y le tic b u t a lso those fo r w h ic h e v id e n c e is to o li t t le fo r m e to m a k e a ju d g e m e n t ; f u tu re w o rk is b o u n d to show th a t som e a r e p a ra p h y le t ic , a n d o th e r s p o ly p h y le tic , a n d th a t a t le a s t som e o f th o se th o u g h t to b e p a ra p h y le tic a re a c tu a lly h o lo p h y le tic .

(2) N a m in g ta x a a n d c la d e s

A n a m e d ta x o n su ch as P ro to z o a o r P la n ta e h a s to se rv e a d u a l ro le . I t s n a m e ac ts a s a la b e l to refer su cc in c tly to a g ro u p o f re la te d o rg a n ism s su ffic ien tly s im ila r to e a c h o th e r th a t th e y sh a re a g e n e ra liz e d p h e n o ty p e , b y w h ic h th e y c a n b e re a d ily reco g n ized a n d d is tin g u ish e d fro m o th e r ta x a . S eco n d ly , th ey a re u n its t h a t c a n b e g ro u p e d to g e th e r h ie ra rc h ic a lly to c r e a te a sm a lle r n u m b e r o f h ig h e r ta x a . A list o f n e s te d c lad e s , su ch as th a t in P a tte rs o n (1 9 9 4 ), c a n b e v e ry u sefu l a s a p h y lo g e n e tic s u m m a ry , b u t i t is n o t th e sam e as a c la ssif ica tio n .

S ta b i l i ty is d e s ira b le in n o m e n c la tu re , so I h a v e tr ie d w h e re v e r re a s o n a b ly poss ib le to r e ta in o ld e r a n d m o re fa m il ia r n am es . B u t s ta b il ity is n o t a p r im a ry v a lu e in c la ssif ica tio n . I f it w ere , w e sh o u ld r ig id ly r e ta in th e o ld e s t c lassif ica tio n ir re sp e c tiv e o f h o w b a d i t is! E sp ec ia lly a m o n g m ic ro o rg a n ism s t r a d i t io n a l c la ss if ica tio n s h a v e b e e n so g ro ssly in c o r re c t th a t th e y m u s t b e c h a n g e d as sc ience

ad v an ces . T h is re q u ire s som e n e w n a m e s o f h ig h e r ta x a a n d som e sh ifts in th e m e a n in g o f o ld ones. B ecause c la ssif ica tio n s a re sc ien tific g e n e ra liz a tio n s a b o u t th e v a r ie d p ro p e r tie s o f o rg an ism s , a n d n o t ju s t in d ex es to s to re d in fo rm a tio n , th e y m u s t be c h a n g e d i f n ew k n o w led g e show s th e m to be fu n d a m e n ta l ly w ro n g . D u r in g th e p a s t h a l f c e n tu ry , e le c tro n m ic ro sco p y , b io c h e m is try a n d m o le c u la r se q u e n c in g h a v e im m en se ly d e e p e n e d o u r u n d e r s ta n d in g o f b io d iv e rs ity . A fte r th e re v o lu tio n a ry ch an g es o ccas io n ed by th is h a v e b e e n so u n d ly a ss im ila ted , o u r c la ss if ica tio n s w ill b e c o m e m o re s tab le . T h u s s ta b il ity is a v a lu a b le o u tc o m e o f a so u n d c la ss if ica tio n , b u t m u s t n o t d o m in a te sy s tem a tic s b y im p e d in g n ece ssa ry ch an g es.

I t is im p o r ta n t to h a v e a b r ie f n a m e fo r a ll c ladcs o f m a jo r e v o lu t io n a ry sig n ifican ce , b u t o n e sh o u ld n o t m ak e th e m is ta k e o f su p p o s in g th a t a ll such c lad e s n eed to b e m a d e in to ta x a . N o r sh o u ld o n e m a k e th e co n v e rse e r r o r , e sp ec ia lly c o m m o n a m o n g c lad is ts , o f su p p o s in g th a t o n ly c lad e s c a n b e tax a . T a x a a n d c la d e s s h o u ld b e th o u g h t o f as tw o p a r t ly o v e rla p p in g sets t h a t se rv e so m e w h a t d if fe re n t, b u t e q u a lly essen tia l, b io lo g ica l p u rp o se s . I n a g iv en c lassifica tio n su ch as th e s ix -k in g d o m system a d v o c a te d h e re , so m e ta x a (e.g . F u n g i, A n im a lia , C h ro m is ta a n d p ro b a b ly P la n ta e ) a re c lad es, b u t p a ra p h y le tic ta x a like B a c te r ia , A rc h e z o a a n d P ro to z o a a re n o t. F o r e x a m p le , a n im p o r ta n t c lad e w h ich is n o t a ta x o n in th is system is th e c lad e co m p r is in g A n im a lia , F u n g i a n d C h o a n o z o a , w h ich I n a m e d o p is th o k o n ta (C a v a lie r -S m ith , 1 9 8 7 A) ; m o le c u la r p h y lo g e n y h a s s ince co n firm e d th e v a lid ity o f th is c la d e (C a v a lie r -S m ith , 1 9 9 3 a ; W a in r ig h t et a i , 1993). I d e lib e ra te ly d id n o t c re a te a ta x o n O p is th o k o n ta o r g ive a d iag n o s is fo r it. T h is is b e c a u se o p is th o k o n ta a r e f a r to o p h e n o ty p ic a lly d iv e rse to b e usefu l as a m a jo r u n i t o f e u k a ry o te c la ssif ica tio n . O n e c lad is t h a s ev en to ld m e th a t I o u g h t to h a v e c re a te d a fo rm a l k in g d o m O p is - th o k o n ta . A k in g d o m O p is th o k o n ta w o u ld be m u c h less usefu l th a n th e ex is tin g k in g d o m s A n im a lia , F u n g i a n d P ro to z o a a s a w a y o f su b d iv id in g th e liv in g w o rld in to m a n a g e a b le m a jo r g ro u p s o f s im ila r o rg an ism s , i.e . in c la s s if ic a tio n a s o p p o se d to p h y lo g en y . T h e c la d is t’s su g g es tio n reflec ts a m isu n d e r s ta n d in g o f th e p u rp o se s a n d fu n c tio n s o f classifica tio n , w h ich is a ll to o c o m m o n a m o n g c lad is ts , w h o a re ty p ic a lly v e ry m u c h m o re in te re s te d in p h y lo g e n y th a n in c la ssif ica tio n , a n d o ften fo rg e t th a t these a re tw o d if fe re n t b ra n c h e s o f system atics . C lad es a n d ta x a a re n o n -e q u iv a le n t c o n cep ts , as is sh o w n p ic to r ia lly in F ig . 3.

214- T . C a v a l i e r - S m i t h

C lades CT Taxa

CTGGTCG

G rades

F ig . 3 . T h e n o n -c q u iv a le n c e o f c la d o s a n d t a x a a n d th e n o n -e x c lu s iv e n e s s o f c i th e r w ith g ra d e s . B io lo g ic a l g ro u p s m a y b e s im p ly c la d e s , g r a d e s o r ta x a , o r a n y tw o o r th re e o f th e se a t th e s a ín e t im e . S o m e w ell k n o w n g ro u p s , su c h a s v e r te b r a te s a n d e u k a ry o te s , a r c s im u lta n e o u s ly ta x a , c la d e s , a n d i m p o r t a n t g ra d e s o f o r g a n iz a t io n ( re g io n C T G ) . S o m e c le a r ly d e f in a b le c la d e s sh o u ld n o t b e m a d e t a x a , p a r t ly b e c a u s e th e y d o n o t c o n s t i tu te c le a r ly d e f in e d g r a d e s o f o r g a n iz a t io n ( re g io n C ) (e .g . o p is th o k o n ta . i.e . th e c la d c c o m p r is in g F u n g i , A n im a l ia a n d C h o a n o z o a (C a v a l ie r -S m ith , 1 9 8 7 a ) ; o r n c o k a ry o te s , th e c la d e c o n s is t in g o f a ll d e s c e n d a n ts o f th e m o s t r e c e n t c o m m o n a n c e s to r o f N e o z o a ) . Y e t o th e r c la d o s a r e g r a d e s o f o r g a n iz a t io n , b u t f o r o th e r re a s o n s a r c n o t m a d e t a x a ( re g io n C G ; e .g . M c ta k a r y o ta , w h ic h w as t r e a te d a s a t a x o n in th e e ig h t k in g d o m sy s te m , b u t n o t in th e six- k in g d o m sy s te m fo r r e a so n s d isc u sse d in th e te x t) . P a r a p h y le t i c ta x a ( re g io n s T a n d G T ) a r c n o t c la d e s ; b u t th e y m a y b e g r a d e s o f o r g a n is a t io n o f g r e a t e r (e .g . B a c te r ia , A rc h e z o a ) o r le sse r (e .g . R e p t i l i a , A m p h ib ia ) im p o r ta n c e ( re g io n G T ) o r th e y m a y n o t b e g r a d e s o f o r g a n iz a t io n a t a ll ( re g io n T ) c i th e r b e c a u s e th e y h a v e s e c o n d a r i ly b e c o m e h e te ro g e n e o u s (e .g . th e h e te r o k o n t ‘ a l g a l ’ p h y lu m O c h r o p h y ta b y m u l t ip le s e c o n d a ry losses o f p la s l id s ) o r b e c a u s e th e y a re to o s im ila r lo r e la te d ta x a to b e c a l le d s e p a r a te g r a d e s o f o r g a n iz a t io n (a s in p a r a p h y le t i c sp e c ie s a n c e s tra l to a l lo p o ly p lo id s , e .g . Spartina anglica a n d S . m aritim a). T h o u g h m a n y h o lo - p h v le l ic ta x a a r e g r a d e s ( re g io n C T G , e .g . T ra c h e o p h y ta ) so m e a r c n o t , b e c a u s e o f s e c o n d a ry c h a n g e s t h a t h a v e c o n v e r te d so m e o f th e i r m e m b e r s to a d r a s t i c a l ly d if fe r e n t g r a d e ( re g io n C T ; e .g . A n im a l ia , w h e r e th e b as ic t r ip lo b la s l ic b o d y p l a n h a s b e e n to ta l ly lo s t b y M y x o z o a ; H e te r o k o n ta w h e r e th e O p a l in a t a h a v e lo s t th e c ilia ry r e l r o n e m e s y n a p o m o rp h y t h a t m a k e s o th e r h e te ro k o n ts a n i m p o r t a n t g r a d e o f o r g a n iz a t io n ) . F in a l ly m a n y im p o r t a n t g r a d e s a r e n e i th e r c la d o s n o r t a x a ( re g io n G ) ; th e y m a y b e p a r a p h y le t i c g r o u p s (e .g . e u b a c te r ia , in v e r te b r a te s , fish ) o r p o lv p h y lc t ic o n e s (e .g . p ro tis ts , z o o i la g c l la te s , a m o e b a e ) . A ll se v e n ty p e s o f b io lo g ic a l g r o u p s h a v e v a lu a b le ro le s lo p la y in th e d e s c r ip t io n a n d a n a ly s is o f o rg a n is m ic d iv e r s i ty ; i t is a s im p lis tic a n d h a r m fu l e r r o r to a t t e m p t to r e s t r ic t th e sc ie n tif ic a lly a p p r o p r i a t e u se o f a n y o f th e m b y n a iv e d ic h o to m ie s in to a l lo w a b le a n d f o rb id d e n ty p e s o f g r o u p , a n d s till w o rse to p r e t e n d t h a t th e th r e e ty p e s t h a t a r e n o t c la d e s a r e n o t e v e n g r o u p s a l a ll.

(3) P r in c ip le s o f r a n k in g ta x a

C lassica lly , ta x o n o m is ts re a c h a co n sen su s o n a p p ro p r ia te ra n k s fo r ta x a b a se d o n a b ro a d k n o w led g e o f d iv e rs ity , ju d g e m e n t o f d e g re e s o f s t ru c tu ra l d is p a r ity , a n d re sp e c t fo r sens ib le t r a d it io n s o f w h a t d eg ree o f d is p a r i ty m e rits a p a r t ic u la r ra n k . T h o u g h ra n k in g h a s a su b jec tiv e e lem en t, i t is a v e ry useful d ev ice fo r h e lp in g th e h u m a n m in d q u ic k ly a p p re c ia te th e r e la tiv e p o s itio n o f n e s te d ta x a w ith in th e ta x o n o m ic h ie r a rc h y a n d , ro u g h ly , th e re la tiv e m a g n i tu d e a n d s ig n ifican ce o f th e d iffe ren ces b e tw een th e m . I t is a m is ta k e to d e n ig ra te th e p rocess o f r a n k in g b e c a u se i t c a n n o t b e o b jec tiv e ly p r o g ra m m e d in to a c o m p u te r .

H u m a n ju d g e m e n t o f s ig n ifican ce a n d rea so n ed ch o ice b e tw e e n a lte rn a t iv e s a re re q u ire d th ro u g h o u t sc ience , as S in g e r (1 9 3 1 : 1 2 1 -1 2 3 ) p e rc e p tiv e ly e m p h a s iz e d ; th e B a c o n ia n e r ro r o f th in k in g th a t on e sh o u ld b e a b le to m a k e im p o r ta n t d iscoverie s o r sens ib le c lassifica tions m ere ly b y p a ss in g fac ts 'th r o u g h a so r t o f a u to m a tic lo g ica l m i l l ’ (S in g er, 1931: 121) is u n fo r tu n a te ly w id e sp re a d a m o n g s t clad ists .

E ven i f w e w ere g iv en th e tru e p h y lo g e n e tic re la tio n sh ip s o f a ll o rg an ism s , c re a t in g a b a la n c e d c lassif ica tio n w o u ld re q u ire ca re fu l ta x o n o m ic ju d g e - m e n t in d e lim itin g a n d ra n k in g ta x a : c lassif ica tio n sh o u ld n o t b e b ased o n a d o g m a tic a p p ro a c h th a t p ro h ib its p a ra p h y le tic ta x a o r a s im p le a lg o r ith m o r ru le lik e th a t o f H e n n ig (1966 ), w h ic h s ta te d th a t th e c a te g o r ic a l r a n k o f a ta x o n sh o u ld b e d e te rm in e d by its b io lo g ica l age . T h e la t te r is p ra c t ic a l ly im possib le , as w e d o n o t know ', a n d m a y n e v e r k n o w p rec ise ly , w h e re th e ro o t o f th e tre e o f life is lo c a te d , a n d th e re a re n u m e ro u s p lace s in th e tre e w ith so m u c h u n c e r ta in ty a b o u t b r a n c h in g o rd e r th a t a t te m p ts to a p p ly th e ru le w o u ld b e a r b i t r a r y a n d less s ta b le th a n th e classica l m e th o d o f ra n k in g b y tax o n o m is ts . If, fo r th e sake o f a rg u m e n t, ive k n ew th a t th e ro o t o f th e tre e o f life w as w ith in th e c y a n o b a c te r ia , w h ich is n o t u n re a s o n a b le g iven th e p a la e o n to lo g ic a l ev id en c e (S chop f, 1993), th e n It w o u ld b e a b su rd to ra n k c e r ta in c y a n o b a c te r ia ) su b g ro u p s m o re h ig h ly th a n th e k in g d o m A n im a lia o r th e su p e rk in g d o m E u k a ry o ta , m e re ly b e c a u se th e y d iv e rg e d e a rl ie r . T h e m o rp h o lo g ic a l a n d c h e m ic a l u n ifo rm ity o f the c y