I ournal of H etpeLology, v ol. 28, No. l, pp. 1 1 4-117, 1994
Copyright 1994 Society for the Study of Amphibians and RePtiles
Sexual Dichromatism in Snakes of the
Genus Vipera: A Review and a New
Evolutionary Hypothesis
Rrcsano SHINE AND THoMAS MADSEN, ZoololgrlDe
p n r t n t t n t , T h e L l n i u e r s i t yo f S V d n e v ,N . S . h . 2 0 0 6 , A r r s
traLta.
T h e s e x e sd i f f e r i n c o l o r i n m a n y s p e c i e so f s n a k e s ,
but these differences are generallv subtle and their
selectiveadvantage (if anv) remains obscure (Shine,
1 9 9 3 a ) .O n e p h y l o g e n e t i c l i n e a g e i n w h i c h d i c h r o matism occurs, and in n'hich the degree of dichromatism varies among closell'-related taxa, is :in the
O l d W o r l d v i p e r i d s n a k e s o f t h e g e n u s V i ; r c r a .T h e s e
snakesare well-suited to an analvsis of the adaptive
significance of dichromatism becausethey are relat i v e l v w e l l - k n o w n e c o l o g i c a l l y .I n p a r t i c u l a r , t h e m o s t
s t r o n g l y d i c h r o m a t i c s p e c i e s ,\ ' / .b t r u s , i s a r g u a b l v t h e
NOTES
most intensively-studied speciesof snake in the world,
and manv populations of this species contain colour
morphs (especially, meianistic individuals) that lack
s e x u a l d i c h r o m a t i s m ( e . g . ,A n d r e n a n d N i l s o n , 1 9 8 1 ;
M a d s e n a n d S t i l l e , 1 9 8 8 ) .I n t h e p r e s e n t p a p e r , w e ( i )
review the distribution and evolution of dichromaLism in ViTtera,and (ii) evaluate a series of alternati.ve
adaptationist explanations for the sexual dichromatrsm.
Species of Vipera occut over a wide area of Europe
a n d t h e M i d d l e E a s t ,i n h a b i t a t s r a n g i n g f r o m a l p i n e
m e a d o w s t o d e s e r t s ,a n d v a r y i n m e a n a d u l t b o d y s i z e
f r o m t h e d i m i n u t i v e V . u r s i r r i i( < 5 0 c m ) t o t h e l a r g e
V . l e b e t i n a( > 1 5 0 c m ) . F e m a l e s g r o w t o l a r g e r b o d y
sizes than conspecific males in some taxa (".9., V.
ursinii, V. berus)but the tevetse is true in others (e.g.,
V . a s p i s ,V . l e b e t i n a S
; t e w a r d , 1 9 7 1 ) .A l t h o u g h c o l o r a t i o n v a r i e s a m o n g s p e c i e s ,a m o n g p o p u l a t i o n s , a n d
a m o n g m o r p h s w i t h i n s p e c i e s( e . 9 . ,N i l s o n a n d A n dren, 1986; Joger et aI., 1992), the rnost common pattern is a brown or grey background color with a series
"zigof cephalic lines running posteriorly into dorsal
zag" markings. In dichromatic taxa,femalesare generally duller in overall color and apparently wellcamouflaged in the natural habitat. Males tend to be
brighter-colored, especially after they slough their
skins, and their dorsal zigzag lines (usually black,
compared to brown in females) stand out more clearly
against the background body color. For example, female V. berus are generally brownish overall with
darker brown zigzag markings, whereas conspecific
males are almost white with black z:gzags during the
m a t i n g s e a s o n ( V i i t a n e n , 1 . 9 6 7 ;P r e s t t , 1 9 7 1 ) . T h i s
bright coloration is evident as soon as males slough,
before they commence mate-searching behavior
(Madsen et aI., 1992). Female V. ammodtltesare greybrown ot reddish-brown with indistinct brown zigzags, whereas males are light grey with black-edged
dark grey zigzag markings (Steward, 1971).Sexual
d i c h r o m a t i s m i s l e s s o b v i o u s i n s e o a r t eai ,n d v i r t u a l l y
absent in the kaznakoui complex (including dinnicki
and dareaskii),ursinii and aspis(Saint Girons, 7978; G.
Nilson, pers. comm.). Although at least slight dichromatism probably occurs in all viviparous V/pera
species, the oviparous Villera (the lcbetiriagroup) iack
dichromatism (G. Nilson, pers. comm.). Two other
forms of dichromatism have also been reported in
s n a k e s o f t h e g e n u s V i l t e r a :( i ) i n V . x a n t h i n a ,v e n t r a l
scales tend to be greyish in maLes, but yellow with
d a r k m a r b l i n g i n f e m a l e s ( S t e w a r d , 1 9 7 1 ) ;a n d ( i i ) t h e
frequencies of different color morphs may also differ
b e t w e e n t h e s e x e s( e . g . ,S t r e e t , 1 9 7 9 ;A n d r e n a n d N i l s o n , 1 9 8 1 ; M a d s e n a n d S h i n e , 1 9 9 2 a ) .F l o w e v e r , t h e
differences in this respect are generaily minor, and
no clear pattern is apparent. Thus, we will not consider these kinds of dichromatism in the following
discussion.
Color differences between male and female vipers
are often subtle, especiallv outside of the breeding
season, and in some cases authorities disagree on
w h e t h e r o r n o t a s p e c i e si s d i c h r o m a t i c ( e . g , V . a s p i s ;
N o b l e , 1 9 3 7 v e r s u s S t e w a r d , 1 9 7 1 ) .S o m e o f t h e s e d i s agreements might reflect the time of year at which
samples are taken (male colors are more intense duri n g t h e b r e e d i n g s e a s o n )o r t h e p a r t i c u l a r p o p u l a t i o n
115
sampled. Geographic variation in the degree of ,1ic h r o m a t i s m h a s b e e n r e p o r t e d i n s o m e s p e c i e s .F o r
example, dichromatism appears to be more extreme
i n s o m e s u b s p e c i e st h a n i n o t h e r s w i t h i n t h e s p e c i e s
V . a m m o d y t e (sG . N i l s o n , p e r s . c o m m . ) , V . u r s i n i i( S t e w ard, 1977) and V. berus (Street, 1979). In some cases,
the situation can be very complex. For example,
northern specimens of V. ranthina tend to be darker
than are specimensfrom more southern populations,
and this trend is more pronounced in females than
in males; thus. dichromatism is more evident in
northern areas whereas snakes of both sexes from
s o u t h e r n a r e a st e n d t o b e l i g h t e r i n c o l o r ( N i l s o n a n d
Andren, 1986).
Phylogenetic hypotheses for Vipera suggest that the
degree of sexualdichromatism is phylogenetically labi1e. For exampJ.e,the two most stronglv dichromatic
t a x a ( V . a m m o d y t e sa n d V . b e r u s )a r e o n l v d i s t a n t l y
related, wheteas the nondichromatic y. rrrsinll is the
s i s t e r - t a x o n t o t h e h i g h l y d i c h r o m a t i c V . b e r u s( e . g . ,
Herrmann et al., 7992). Thus, the dichromatism seen
within this lineage cannot be dismissedas being due
to phylogenetic conservatism (retention of ancestral
features). A molecular phylogeny for the viperine
snakes-iirdicatesthat the outgroups (Cerastesand Eclris)
a n d b a s a l t a x a i n t h e i n g r o u p ( l e b e t i n ar,a n t h t n a ,u r s i t i i )
are essentially nondichromatic (fig. 2 of Herrmann et
al.,7992). This phylogenetic hypothesis suggests that
dichromatisrn has evolved independently at least
twice: once inberus and once in the amntodylesgroup.
Alternatively, dichromatism may have evolved only
once (basal to the lterus-annnodytes-aspis
clade) and
subsequently been lost twice (in nspisand the dirtnickikaznakoailineage).Two Iines of evidence indicate that
it is the coLorationof adult males rather than adult
females that has become modified through viperine
phylogeny: (i) females in dichromatic Vipera species
resemble both sexes of related nondichromatic vip e r i n e s p e c i e si n c o l o r , a n d ( i i ) b r i g h t m a l e c o l o r s i n
dichromatic taxa are restricted to the mating season.
Thus, we proceed to consider adaptationist hypothe s e sf o r t h e e v o l u t i o n o f b r i g h t c o l o r s i n r e p r o d u c t i v e
male viperines.
Evolutionary theory suggests two processes-sexual selection and/or natural selection-that could
c o n f e r a s e L e c t i v ea d v a n t a g e t o b r i g h t c o l o r a t i o n i n
male Vipera.In turn, sexual selection is divisible into
two main forms, intrasexual and intersexual. Bright
nuptial colors in several species of male lizards are
clearly attributable to intrasexual selection: for ex"green
badge" of reproductive male sand
ample, the
bzards (Lacerta a,gi/i-s)serves as a signal of a male's
fighting ability, and is used by other males to evaluate
the probable outcome of a combat bout (Olsson,1992).
Male Vipera of several species (probably, all species)
d o s h o w m a L e - m a l ec o m b a t ( r e v i e w i n S h i n e , 1 9 9 3 b ) ,
but field studies provide no indication of color ass e s s m e n tb v r i v a l m a l e s p r i o r t o c o m b a t , o r a n y i n c r e m e n t i n c o m b a t s u c c e s sd u e t o b r i g h t c o l o r s . T h e
most detailed data in this respect come from comp a r i s o n so f m a l e a d d e r s o f t w o c o l o r m o r p h s i n a s m a l l
population at Smygehuk in extreme southern Sweden
( M a d s e n a n d S h i n e , 1 9 9 2 a ) .A l i h o u g h " b l u e " m a l e s
"normal"
are duller in color than
males, they show
in
reproductive
success (Madsen and
no dectease
tt6
NOTES
S h i n e , 1 9 9 2 a ) .S u c c e s si n c o m b a t a p p e a r s t o d e p e n d
a l m o s t e n t i r e l y o n a m a l e ' s b o d y s i z e ,w i t h c o l o r b e i n g
irrelevant in this respect (Andren and Nilson, 1981;
M a d s e n a n d S h i n e , 1 9 9 2 a ) .T h e s e d a t a t h u s s u g g e s t
that intrasexual selection is not resDonsible for the
d i c h r o m a t i s mo b s e r v e di n V . l c r u s .
Intersexual selection might also favor dichromatism, if receptive females actively select more brightly-colored males. Female preferences may well have
been responsible for the evolution of bright male
c o l o r s i n m a n y t y p e s o f a n i m a l s ( e . g . ,K r e b s a n d D a vies, 1991), but seem unlikely to be imporiant in
s n a k e s .C o l o r d i s c r i m i n a t i o n h a s n o t b e e n s h o w n i n
t h e s ea n i m a l s , a n d o u r s t u d i e sa t S m y g e h u k s h o w t h a t
the dull "blue" males are more successful than similar-sized"normal" maies (Madsen and Shine, 1992a).
Indeed, "blue" males can actually induce mating (female receptivity) after briefer courtship than can
"normal"
m a l e s ( M a d s e n a n d S h i n e , 1 9 9 2 a ) .C o m parisons of "normal" and melanistic males have also
failed to reveal any advantage to the more brightlycolored morph (Andren and Nilson, 1981).In combination, these data suggest that dichromatism in Vi,
pera cannot be attributed to sexual selection. We also
note that mating systems appear to be phylogenetically conservative within Vipera so that the high degree of interspecific and intraspecific variation in the
degree of dichromatism observed in this group would
not be expected of a sexually selected trait.
Could viperine dichromatism evolve via natural
selection rather than sexual seLection? At first sight
this possibility seems unlikely, because the only selective forces that would favor the dichromatism
would involve ecological differences between males
and females. Dietary analyses show no consistent differences in prey types taken by male and female adders
( P r e s t t , 1 9 7 1 ) :i n d e e d , m a l e s d o n o t e v e n f e e d d u r i n g
the mating season, when the dichromatism is most
i n t e n s e ( M a d s e n a n d S h i n e , 1 9 9 3 ) .T h e r m o r e g u l a t o r y
differences between males and females are also likelv
to be minor at this time of year, and studies on garter
snakes suggest that dorsal reflectances (and thus,
heating rates) will differ only slightly between the
sexes (Gibson and Falls, 1979). However, male and
female adders do differ substantiallv in movement
p a t t e r n sd u r i n g t h e m a t i n g s e a s o n M
. alesmove large
distances in search of receptive females, often across
relatively open habitats, whereas females are highly
sedentary and tend to remain in more sheltered areas
(e.g., Viitanen, 1967; Prestt, 1971; Andren, 1985, 1986;
M a d s e n a n d S h i n e , 1 9 9 2 b ) .M o v i n g a d d e r s a r e m o r e
vulnerabLe to predators (especially, birds) than are
stationary adders (Andren, 1985; Madsen and Shine,
19 9 3 ) .
Is there any plausible reason why bright colors
might enhance a moving snake's ability to evade
predators? Superficially, it seems as though bright
coloration would be a particularly great disadrantage
to a reproductive male adder: at least to a human
observer, males are very obvious during the mating
s e a s o n( A n d r e n , 1 9 8 5 ;p e r s . o b s . ) .N o n e t h e l e s s ,s n a k e s
of many species have evolved brightly-banded patterns that apparently function to confuse visuallyhunting predators by inducing "flicker-fusion." This
phenomenon occurs when the images of the bands
move across the predator's eyes at such a speed that
it becomesdifficult to focus on the moving object or
t o a s s e s si t s v e l o c i t y o r d i r e c t i o n o f m o v e m e n t ( J a c k s o n e t a 1 . , 1 9 7 6 ;S h i n e , 1 9 8 0 ) . I n t h e c o u r s e o f o u r
fieldwork on adders, we noticed the same effect with
fast-moving male snakes.The black zigzag marks stand
out against the pale background color, and function
like bands as the snake moves rapidlv. The end result
i s a b l u r i n w h i c h t h e s n a k e ' se r a i t p o s i t i o n i s d i f f i c u l t
to ascertain. If natural predators experience the same
phenomenon, the bright contrasting colors of male
adders may actually enhance the snakes'survival as
they move about rapidly in search of mates.
"flicker-fusion"
The
hvpothesis is consistent with
t h e f a c tt h a t t h e b r i g h t . o i o . . n r e s h o w n o n l y b y a d u l t
males, and only during the mating season. Matesearching males have been reported to show very
extensive movements in several studies of adders (e.g.,
Viitanen, 1967; Andren, 1985, 1986; Madsen et a1.,
1 9 9 3 ) .J u v e n i l e s ,a d u l t f e r n a l e s ,a n d n o n - r e p r o d u c t i v e
male snakes all adopt more sombre hues, and our
o b s e r v a t i o n sa t S m y g e h u k s u g g e s t t h a t t h e s e a n i m a l s
are relatively sedentary and hence rely on camouflage
rather than predator deception (e.g., Madsen and
S h i n e , 1 9 9 2 b ) .T h e s e a s o n a lt i m i n g o f m a l e s l o u g h i n g
relative'to mating activity may also be important in
the evolution of dichromatism. If mating follows
s l o u g h i n g ( a si n V . b e r r sa n d t h e d i c h r o m a t i c m o n t a n e
p o p u l a t i o n s o f V . a m n t o d y t c sG
; . Nilson, pers. comm.),
males will tend to be brighter than females even without any adaptive modifications of male color. Thus,
there will be abundant color variation upon which
n a t u r a l s e l e c t i o n c a n o p e r a t e ,a n d t h e e v o l u t i o n o f
dichromatism may be facilitated. We predict that the
extent of color variation among males will be .lower
in taxa (such as V. nspis)in which mating is not linked
to male sloughing (Saint Girons, 1957).
"flicker-fusion"
Although the
hypothesis thus offers a plausible explanation for the adaptive significance of sexual dichromatism in Vipera berus,the hypothesis is a difficult one to test. Experimental
m a n i p u l a t i o n o f m a l e c o l o r s ,w i t h m o n i t o r i n g o f s u r vival rates, would be the best technique for such a
test but imposes major logistical difficulties. Plasticine
models of different colors have proven useful in testi n g s i m i l a r h y p o t h e s e s( A n d r e n a n d N i l s o n , l c 8 l ;
Andren, 1985; Olsson, 7992), bttt are inapplicable in
the present case because our hypothesis relies on
movement by the snakes. Comparative behavioral
studies on supposedly non-dichromatic populations
of V. berus, or on other Vlpera species with both dichromatic and non-dichromatic subspecies would be
useful also. Vipera ammodyteslooks to be particularly
interesting in this respect, because it shows geographic variation both in the degree of dichromatism, and
in the seasonal timing of its mating activity (G. Nilson, pers. cornm.). We predict that populations with
differing degrees of dichromatisrn will differ also in
the degree to which mate-searching males experience
mortality due to visually-hunting predators.
Acknowledgmenls.-We thank G. Nilson for comments on the manuscript, G. Nilson and C. Andren
for sharing their extensive knowledge of Vtpera brology, and the Australian Research Council for financial support.
NOTES
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Accepted: 26 October 1993.