BwlogicalJournal ofthe Linncm Society (1981),16: 213-259. With 1 figure
The genetics of colour-patternsin the
grasshopper Chorth@w brunneus
PETER GILL
Department of Genetics, University of Nottingham,
Nottiniham NG7 2RD
AcceptedfmpublicationJunc 1981
Several alleles were found to determine the colour of the dorsal pronotum in Chorthipp bnuutnrs;
there was evidence for at least two loci (C and V). Brown (C.)was the universal recessiveandgreen(@)
was dominant to all other colours. The white allele (C9,was codominant with green(@)and purple
(C"").Wing-patterns were determined by a separate, probably linked locus (W). A dominant plain
wing-pattern(Wqwas associated with colours other than brown. Striped( W)and mottled( *)were
codominant and a plain recessiveallele (W)was also found. All three alleles were associated with the
brown phenotype. A purple-sided allele (Sh)was sometimes o b m d with Cp...P was dominant to
brown sides (P),A series of markings on the dorsal and lateral pronotum (hma i n t m d i a , fa&
postocularis, linra media, caritur media and M M latrralic) were investigated and found to be controlled at
separate loci which may be linked to W.These characters were expressed by dominant alleles.
Epistatic effects by modifier loci were shown to have an important effect on the determination of
wing phenotype. Allele Wo+, for example, suppressed the stripe-wingpattern, hnca media, cmina mdia
and LOW lateralis.
It was concluded that colour patterns appear to be under geneticcontrol and that dominant alleles
were rare in the wild. Changes in shades of colours were shown to be age-dependent and minor.
KEY WORDS:-Chmthippus
brunneus
- colour-patterns - genetin - dominance - epistasis.
CONTENTS
Introduction
. . . . . . . . . . . . . . .
Methods
. . . . . . . . . . . . . . . .
Colour of the dorsal pronotum . . . . . . . . .
Colour of the pronotal side and femur . . . . . . .
Wing pattern . . . . . . . . . . . . . .
Wedge . . . . . . . . . . . . . . . .
Lines
. . . . . . . . . . . . . . . .
Results
. . . . . . . . . . . . . . . . .
Locus C (colours) . . . . . . . . . . . . .
Allele P(green dorsal pronoturn)
. . . . . . .
Alleles C""and CR(purple and red-brown dorsal pronotum)
Allele c" and locus V (whitedorsal pronoturn) . . . .
Allele CN(blackdorsal pronotum)
Allele CB(brown dorsal pronoturn)
Locus S (Pronotal side coloration) . . . . . . . .
AllelesSB,P,Wbrown, purple and green phenotypes)
.
Locus F(Hind-femoral coloration) . . . . . . . .
Alleles FA,P,Fc . . . . . . . . . . . .
.
.
.
.
.
.
.
.
.
.
.
.
. . . . . . . .
. . . . . . . .
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
. . . . . .
. . . . . .
. . . . . .
. . . . . .
. . . . . . .
244
244
244
244
244
244
245
246
246
241
247
247
241
241
250
250
250
250
243
0024406618 !I070243
+.17iS02.00/0
Q 198 1The Linnean Society of London
P. GILL
244
. . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
Locus W(wing-panerns)
AlleleW(plainwing-pattcm)
Allele W(recessive Lainwing-type)
Alleles w k and M+ kottled wing-type)
Allele W(stripedwing-type)
LocusWo(wedgemark)
Alleles WO’, woLines
LocusLil(lincain&nudia)
LocusFp~~ciupactonclmi~
Loci Lm and Cm (linaamedia and ccuina media)
Locus 22 hma &tmaliI)
Discussion . . . . . . . . . . . .
Epistaticandlinlragerelationships
Dominancerelatiohhips
ColourchangesinOrthoptera
Adaptive signihcance ofcolour-pattern variation
Acknowledgements
References . . . . . . . . . . . .
. .
. . . .
. . . . .
. . . . . . . . .
. . .
. .
. . . .
.
. . .
. .
. . . . . .
. .. ..
. . . . . . . . . . .
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
. . . . . . . . . . .
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
. .
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
250
25 I
25 1
25 1
25 1
25 1
25 1
253
253
253
253
253
256
256
256
258
258
259
259
INTRODUCTION
Although differences in colour- atterns in s ecies of British grasshoppers are
well known (Ragge, 1965; Richar s and Walog 19541, little is known regarding
their inheritance. Addidue are well known to be able to change their colours in
response to environmental or physiological factors such as temperature
(Goodwin, 1952; Key 8c Day, 1954), crowding (Stower, 19591, changes in
background colour (Uvarov, 1966) and ageing or maturation (Burtt 8c Uvarov,
1944). Evidence for the inheritance of colour-patterns involving epistasis in
Chorthippwpurullelurw a s provided by Sansome 8c La Cour ( 1935). Nabours ( 1929),
Nabours 8c Kingsley (19341, Nabours, Larson 8c Harh6g (1932) investigated the
inheritance of colour-patterns in grouse-locusts (Tettigidae)finding a series of
closely linked loci.
B
METHODS
Grasshoppers were reared according to the methods of Kelly-Stebbings &
Hewitt (1972) except that nymphs and adults were kept in a constant temperature
room at 25OC and radiant heat was supplied by 100 W light bulbs. The only food
supplied w a s Ductylis glommutu. A 12 h photoperiod was maintained.
Characters were scored following the methods of Ragge (19651 and the
following were noted (Fig. 1).
Colour ofthe dorsd pronotum: Major colours observed were green, purple, white,
black and brown. The brown category consisted of shades ranging from grey to
dark brown. A colour atlas w a s used in identifyingshades (Kornerup8c Wanscher,
1963).
Colour ofpronotul side andfemur. There were two scorable categories-purple and
brown.
Wingputtem. Different wing-types observed were plain, light-mottled, mottled,
stripe-mottled and striped. Plain-winged individuals had no visible markings ;
light-mottled had only faint markings whereas mottled were heavily marked;
stripe-mottled individuals had both characters evident.
Wedge: This dorsal pronotum marking was scored by its presence or absence.
GENETICS OF COLOUR-PATTERNS IN C. BRUNNEUS
245
Table 1. List of loci and alleles showing symbols used in text and Tables 2-6
Allele
Locus
C
Character affected
Colour of dorsal pronotum
Effect
brown
black
red-brown
Purple
green
V
S
F
W
Colour of lateral pronotum
Colour of upper hind femur
Wingtype
white
white
brown
brown
PUrplc
Brem
brown
Purple
green
plain (recessive)
mottled
light-mottled
Striped
Q
M
L
T
WO
Lit
FP
Zl
Lm
Cm
I
IF
J
K
N
Wedge
plain (dominant)
plain
no effect
mottled
no effect
mottle suppressor
no effect
stripe suppressor
no effect
wedgeless
wedged
Symbol
Phenotype
Genotype
C'
CBl
CB
P
CR
C"
CQ
c"
co
CW
CW
C'
S'
C'u
CW
V+
VSB
Sh
SO
Sfi
'F
FB
P
P
so
WQ
F"
Fo
WI
w""
W"'
WS'
W
'
WQ
Q-
Q'
Q-
w
F
W'"
v
F
ML+
LT+
Two+
wo-
M+
ML+
LT+
T-
wo
+
wo-
Linea intennedia
Fascia postocularis
Zona lateralis
Linea media
Carina media
character expressed
no ettect
+-
-
Linea intennedia
Fascia postocularis
Zona lateralis
Linea media
Carina media
character suppressed
no ett't
-+
+-
+
Lines: Other markings scored for absence or presence I name collectivelyas lines
and include linea media, carina media, Lima intennedia and farciapostocularis on the
dorsal head and pronotum; the z m lateralis on the ronotum side.
A complete list of loci, alleles and symbols used in tRe text are given in Table 1.
Crosses between unlike and like phenotypes were carried out in order to
determine the inheritance. Parent-offspring backcrosses could not be carried out
because of the relatively short life-span of the adults, although three generations
per year could be raised so that sib matings over several generations could be
carried out. Adults used in crosses were separated by sex before the final instar to
ensure that females were virgin. The results ofcrosses are shown in Tables 2-6. For
each cross, genotypes are given. Frequencies were tested usingX4and significance
was taken as P < 0.05.
246
MMkd
1
stripad
W h portcm
Figure 1. Marking and wing patterns of C. bnmMu (after Ragge, 1965).
RESULTS
Locus C (colours)
Colours were scored from the dorsal pronotum. Usually, the wing was of the
same colour, although some caution was required because the wing and pronotum
were sometimes different. A green pronotum w a s often found with straw coloured
GENETICS OF COLOUR-PATT'ERNS IN C. ERUNNEUS
247
wings in young adults, but laying down of green pigment appeared to be active at
least during the first week of adulthood so that the green-wing coloration often
developed with age. This usually occurred with a general darkening of the
pronotum.
The classification of colours in this paper is not definitive-the brown colour
covers a wide range of shades from grey to dark brown with numerous intermediates. These may be determined by multiple alleles but undoubtedly there is
some phenotypic variation, such that a given genotype is capable of producing a
range of shades in the adult. It is justified, therefore, to sim lify classificationsof
brown colours until they can be investigated more thorough y. Similarly, different
shades of green, purple, black and white have been incorporated together in this
preliminary work.
Allele CG (green dorsal pronoturn). This allele confers a green colour to the dorsal
pronotum. CGwas probably dominant to all other colours investigated (Table 2).
Mating 4, for example, produced approximately 1 : 1 greedbrown phenotypes
Cxz= 0.063, P > 0.05).Subsequent F, generations ( 5 and 5B) and F, generations
(5Aand 5C) confirm dominance of green over brown. Matings 6B, 7A, 7B, 9,10,11
show dominance of green over purple (alleleCp,)
and red-brown(CR).In matings
6B, 10 and 11, crosses between cGCGand C W B or CRCBheterozygotes produced
grasshoppers showing only the green phenotype. ChcG heterozygotes were
recognizable, however, by their darker shade. In the presence of purple side (allele
Sfi; crosses 7A, 7B), the green colour was darker still and completely masked in
nymphs and adults less than five days old. The dorsal pronotum and wing colours
in these individuals were dark brown (5F8 in the colour-atlas of Kornerup &
Wanscher, 19631, suggesting codominance of C f i with Cc in the presence of S f i .
Gradually, green pigment was laid down preferentially to purple, but the final
colour observed was a dark shade of green (3OF41-the usual colour was 29ES.
In mating 2, 1 brown: 26 individuals were observed after mating 2 green
parents. This may suggest the influence of a second locus.
Alleles C f i and CR (purple and red-brown dorsalpronoturn). There were at least two
alleles producing purple type colorations. The commonest was bright-purple
( 1 1E8 in the colour-atlas); matings 6, 6A and 6B involved crosses of red-brown
(7F8) phenotypes. Mating 7A showed that C f i was dominant to CR (xzof
observedlexpected frequencies = 3.86 for 2 d.f., P > 0.05). Both Ch and CRwere
dominant to CB(matings6A, 7A, 7B).
Allele C W and locus V (white dorsal pronotum). Two loci (Cand V )were postulated
having alleles C W and V+, producing a white dorsal pronotum. Alleles W a n d V+
were dominant to brown but codominant with purple(Cp,)and green(P)(matings
8 and 8B). CWCh or V+Cpu heterozygotes were light pink ( 1 13B in the colour-atlas)
and the wings had a pink flush, whereas CwCGorV+Cc genotypes had a light green
pronotum (30A5)but the wings were white in all but two individuals and no green
coloration was visible in the nymphs.
Mating 8 may suggest the presence of two loci (C and V )because excess white
individuals were observed (x2=4.96, P < 0.05 for 1 d.f.-purple + pink were
compared with white usinga one locus model;X*= 1.7 7, P > 0.05, using two loci).
Allele CB1(black dorsalpronoturn). Mating 1 indicates that P i s dominant to P a n d
resulting in the ratios 2 green: 1 black: 1 brown (x*=1.75,P>0.05).
Allele CB (brown dorsal pronoturn). As has already been indicated, the brown
phenotype is probably controlled by two or more alleles. Interpretation is
P
17
cowc
COW(sj x COWisj
C
B
W (4) x CBW- (4)
cod
7A
5D
C O S " d (68) x P S h d (7)
bv
(5B) *
C B W(5B) x (.?
C B W(17A) x C(SB)
6
C ' W W xd d
(WoodfordGreen) (Epping Forest 2)
6A
c " p (6) x b d (6)
6B
(6A) x C O d ( 5 )
7 C h S h d (Leyton 2) x C'S'W (amber2)
5A
5B
5c
(Epping Forest 2) (Epping Forest 2)
(4) x
14)
5
Male
CBW-XCOW
Phenotype
CBW-(l)XCBW-(l)
Cd (Kimberley) x COW (Shipky)
COW (shipley)x P d (shipky)
Female
1A
2
3
4
Mating
Possible genotype
Striped
-
-
-
-
-
9 C'
15 CB
-
X'
26C', 1 C?
-
1COWO'
8 CB
3ewo-,
1 CBWo',
cob,
4c"
32 CO
8P S B ,
12 chs"
6P S h ,
3P S B .
5 PCOS",
2
5 C"SB
2 CQ"SB,
8P S P " ,
4 ,C"C%h,
17 C%',
17'
S
'
C
3c",2CB
22cs
11 CO
14C?
1CS
6 CB
26 ?C
4CO,7P
2C?, 32CO
4 COwo+
Wing phenotypes of progeny
Mottled
Stripamottled
Plain
Light-mottled
Table 2. Crosses showing inheritance of wingtype and colour loci C, D, W , Wo, S, M yL, T, V, Q. Origins of parents are given in
parentheses. Geographical locations are listed by Gill (1981)
19A
18D
18E
19
18C
18A
18B
16A
17
17A
17B
17C
18
15A
16
15
14
12A
13
8A
8B
9
10
11
12
8
C?w
CwW"x C"W (Kimberley)
(Epping Forest 2)
ChCwW (8) x cp"cwW(8)
COWp ( 5 ) x CWW(8A)
CGW ( 5 ) x C h W (Dovedale)
CGW ( 5 ) x ChW (Dovedale)
( 5 ) x Cpyw
(Dovedale)
C'W' x c w w p
(Epping Forest 1) (Epping Forest 2)
CW
' m
' O (12)x C'W" (12)
C'W' x C ' W F
(Woodford Green) (Woodford Green)
C"W x C'W' (Shipley)
(Epping Forest 2)
C ' W F (Shipley) x C B W P
(Epping Forest 2)
b W F (15)x C ' W F (15)
C'W x cw(Epping Forest 2) (Epping Forest 2)
CBF(16)xC'W''"''(16)
C'W (?) x C ' F (nkeston)
C'W (17)x CW
' Illlo (17)
C ' W F (17)x C'W'lllo (17)
C'w (17B) x C'W (17B)
C ' W F x C'W
(Epping Forest 2) (Epping Forest 2)
C " V (18) x C ' V (18)
C'WWo+ (19)x C B p(18)
C ' F W o * (18B) x C ' F W o + (18B)
C ' W F (18C)x C'W (5D)
C'W (18B)x C'W (18B)
C'FWO+ x C ' F W o (Epping Forest 2) (Epping Forest 2)
C'W' (19) x C ' V (1)
COPV
cwcpyv
3 C"
1C"
2 C'
4 CB
8 C'Wo+
20 b w o +
17 C'wo',
2 PWO'
7 C'
3 b
6 C'Wo-
-
1 C'Woscwo6 CB
2 C'
1 C'
2 CB
-
6 C"
-
13 C"
6 C'
4 C"
4 C'
2 C'
5 C'. 1 CP"
17 C"
6 C'
-
3 c'wo
-
7 C'
7 C'
3 c'
1 c'
5 C'
1 C'
3 C'
-
4 C'
-
5 C"CW
1 C", 4Cw
13C?Cw
6 C ? , 2Ch
32 CG
24cG
5cw
1 cpu, lOCW,
-
7 C'
1 cnwo-
11 C'
5 C'
3 C'
5 C'
9 C"
3 c"
5 C'
P. GILL
250
rendered difficult because minor colour changes can occur, especially in the
recently emerged adult and secondlybecause crossesbetween two shades of brown
or grey tend to produce a confusing range of brown colour- es. However, none
of the matings between brown individuals produced any o the colours already
discussed which indicated the recessiveness of the brown genotype. Work is in
progress to analyse the allelicrelationships of the CBcomplex.
rp
Locus S (Pronotal side coloration)
Alleles SB, Sh,SC (brown, purple andgreenp h t y p e s ) . Matings 7,7A and 7B involved
. was rare in the wild (Gill, 1981)
crosses of purple-sided individuals (alleleP)Sfi
but was always found associated with a purple dorsal pronotum ( C f i ) .Breeding
experiments (Table 2)suggested that Sfiwas dominant to brown sides (SB)butwas
only expressed in the presence of C f i . In the absence of linkage and assuming
crosses 7, 7A and 7B were
CuPuSpll
CGorBorRSB
,
CBSB
CBSB
then equal numbers of'CfiSBand CAtsPu individuals would be expected in each
progeny, but in fact a total of 25 individuals were CfiSfi and 13 were CfiSB
(x4=3.78, P=0.1-0.05), therefore, although linkage of Cand S may be
indicated, further data are required.
Individuals with CfiSfiphenotypes are brightly coloured in the nymphal stages
but when the adult stage is reached, the intensity of the purple colour on the side of
the pronotum becomes markedly less.
Ragge ( 1965)noted the existence of an extremely rare green-sided variety. None
were observed by Gill (1981)but it is reasonable to speculate that this condition
was caused by another allele (F);
it is possibly only expressed in the presence of CC
and may be dominant to Sh .
Locus F (Hindfmoral coloration)
Alleles P,
P,Fc.In breeding experiments 7, 7A and 7B, all progeny with purple
pronota or CWfi/CGSBheterozygotes had a purple flush to the hind-femora
whereas all other individuals did not show this character, suggesting either close
linkageofallele P with Cfior allele C f iitself may cause the purple coloration ofthe
hind-femur. ChSB/cGss individuals (matings 9, 10, 11) lacked the purple femur
indicating that S i n theabsenceof CfiSfiwill inhibit P.
Locus W (wing-pattenas)
Locus W determines the wing-pattern. Five patterns were scored: plain, lightmottled, mottled, stripe-mottled and striped (Fig. 1). The variation of mottling on
the wing appeared to be continuous, hence in some cases plain and light-mottled;
or light-mottled and mottled varieties may be the same. Examination of the data in
Table 2 may suggest confusion in scoring light-mottled and mottled phenotypes,
hence for the purposes of genetic analysis these have been combined and treated as
GENETICS OF COLOUR-PATT'ERNS IN C. BRUNNELIS
25 1
the product ofa single allele( Wmo),although it is likely that two or more alleles exist
which produce a range of different mottled phenotypes.
Allele W (plain wing-pattern). This allele was dominant and associated with
colours green, purple, white and red-brown e.g. matings 6B (green-plain
dominant to striped wing pattern); 8 (plain dominant to mottled and striped); 7
(purple-plain dominant to brown-mottled). Linkage of W with C was suggested
since occasional recombinants were recorded (matings 4, 6, 8, 10).
An additional locus (Q)may be associated with locus V which produces white
pronota (matings 2, 8A). Allele Q+ may be linked to V+,producing white plainwinged phenotypes.
Allele WP (recessive plain wing-type). The plain wing-pattern was also observed in
brown grasshoppers but on breeding appeared to be recessive (e.g. matings 5B,
5D, 12A, 14, 16A, 17A, 18E). None of the parents of F, generations had the plain
wing phenotype.
Alleles w"" and M + (mottled wing-type). Allele Wmo probably consists of two or
more alleles which produce different amounts of mottling (Table 1). The
combination WmowP may tend to produce light-mottled individuals. W ois
the heterozygote producing the intermediate stripe-mottled
codominant with W1,
phenotype (e.g. matings 3 , 6 , 13, 15, 15A). However, there were indications of two
modifier loci which affected mottling of the wing. Matings 16 and 18 produced
phenotypes which could not arise from a single locus; a second locus ( L )which
reduced the amount of mottling on the wing was indicated.Whto WL'L- produced
a plain wing-type and WmoWhoLtL-produced a light-mottled wing (x* for mating
16 = 0.73 for 3 d.f. and for mating 18 x* = 2.059 for 4 d.f., P > 0.05).
Mating 18D suggested a separate locus (MI which converted the striped to a
stripe-mottled phenotype but had no effect on the plain-wing ( W ) - X *= 1.36 for
2 d.f., P > 0.05.
Allele W 1
(striped wing-type). This allele produced a striped wing attern (Fig. 1)
which was codominant with alleles whoand M+.There was good evi ence of at least
two modifier loci which completely inhibited the expression of W t These
.
were Wo
and T, the former also inhibiting expression of the wedge mark (Fig. 1) and hence
easily identified. In mating B1, between WmoWo+parents,striped and stripemottled offspring were recovered, indicating that the parental genotypes were
WS'WoWo+wo-.
Matings 1 7 and F, mating ( 17B) could be explained by the influence of either
allele Tt, which converted striped to plain or light-mottled patterns, or by the
mottled-wing locus ( M ) . Famating (l7C) confirmed the presence of a stripe-wing
suppressor, however this was not significant statistically (x*=2.73 for 2 d.f.1.
B
Locus Wo (wedge murk)
Alleles Wo+, Wo-. Wo+supressed wedge marking (Fig. 1) and was dominant to
Wo- (matings 1, 18B, 18C and 19; Table 2). There was no evidence oflinkage of Wo
with any other locus. In a mating between a wedgeless black individual and a green
wedged grasshopper (mating l), wedgeless individuals having green, brown or
black phenotypes were recovered. Wo+suppresses the striped-wing pattern, linea.
media, carina media and rona lateralis.
xW t +
*Lit+ x d L i t +
*Lit+ x m t -itx -Lit+
m t +xm t mit-x Wt+
8B
-itxW t +
9
mt-x m t w 2 i t - x -it10
11
mit-x W t 12
W L i t + x -it+
12A
x W-t*LitWLit+ x WLit13
14
WLit- x W i t +
W F L i t +xW F L i t 15
*-Lit+
x W-it
+
15A
*Lit+ x w"Lit+
16
V L i t - x *Lit+
16A
*Lit+ x -Lit17
w"Lit+ x W L i t 17A
W F L i t + x WhOLit+
17B
W a F L i t + x WPLit18
18B W"OLit-Wo+ x W L i t + w o 18C F L i t - W o + x w"Lit+Wo+
6
6A
6B
7
8
8A
*-it-
phenotype
Mating Femak
M&
PossiMc genotype
-
5 Lit+
-
2 Lit1 Lit-, 8 Lit+
-
1 Lit-. 3 Lit+
-
3 Lit-
6 Lit+
6 Lit+
5 Lit+
5 Lit+
-
1 Lit+
2 Lit-, 3 Lit+
4 Lit+
striped
Light-mottkd
2 Lit-, 3 Lit+
4 Lit+
16 Lit+, 16 Lit10 Lit+
20 Lit6 Lit6 Lit-, 10 Lit+
2 Lit-, 3 Lit+
2 Lit-, 11 Lit+
7 Lit-, 1 Lit+
25 Lit-, 7 Lit+ 6 Lit-, 1 Lit+
19 Lit-, 5 Lit+
1 Lit+
1 Lit-, 4 Lit+
4 Lit2 Lit1 Lit+
4 Lit4 Lit4 Lit-, 2 Lit+
2 Lit-, 1 Lit+
2 Lit-, 11 Lit+
5 Lit1 Lit-, 5 Lit+
3 Lit-, 1 Lit*
3 Lit+
3 Lit-. 2 Lit+
3 Lit-, 4 Lit+ 9 Lit-. 2 Lit+
1 Lit1 Lit-. 2 Lit+ 6 Lit-, 1 Lit+ 3 Lit-. 2 Lit+
2 Lit-, 1 Li+ 1 Lit-, 2 Lit+
2 Lit+
1 Lit3 Lit-, 2Lit+
2 Lit+
2 Lit1 Lit3 Lit4 Lit-, 4 Lit+
1 Lit1 Lit+
3 Lit17 Lit-, 3 Lit+
5 Lit+
2 Lit+
Wing phenotypes of progeny
Stripamotded
Plain
Mottled
Table 3. Crosses showing the inheritance of the Lineu intennedk (Lit).Crosses not listed did not have Lit+ in either parents or progeny. See
Table 2 for origins of parents
GENETICS OF COLOUR-PATTERNS IN C. BRUNNEUS
253
Lines
Loci Lm, Cm, Lit, Fp and Z1 were known collectively as lines. The presence of
characters scored were dominant to their absence. Results are given in Tables 3-6.
In all cases + represents the dominant allele. All loci were affected by modifiers.
Locus Lit (linea intermedia)
Lit+ produced a pale to dark coloured line behind the eye (Fig. 1)and was predominantly associated with striped or stripe-mottled wing-types (Table 3).WPLit+
individuals were observed in progeny of matings 6,6A, 6B and 8, however. Mating
18B confirmed that allele Wo+ did not inhibit Lit+ as Wo+Lit+offspring were
observed. Association of Lit+ with Wt was suggested by mating 18C in which
WStLit + Wo - individuals were recovered.
In mating 16, a rare mottled/lit+ male was crossed with a sa-ipedllit- female.
The resulting stripe-winged progeny did not show the Lit+ phenotype suggesting
linkage of'Lit with W . Accordingly, expected frequencies of' progeny in table were
calculated (xz= 25.73 for 4 d.f., P < 0.001).
In matings 9, 10 and 1 1, crosses between individuals which did not show a linea
intermedia were carried out and resulted in Lit+progeny. This implied the presence
of an inhibitory locus ( I ) . xp of frequencies were not significantly different
( P > 0.05) to those expected using a two locus hypothesis.
Locus Fp uascia postocularis)
Fp+ produced a grey coloration between the linea intermedia and the eye. Because
thefasciapostocularis forms a boundary at the position of the linea intermedia, Lit+Fp+
individuals could not be distinguished from Lit-Fp+. Lit and Fp were probably
linked because excess Lit+ individuals were not recorded in Table 3. Occasional
crossovers were observed in which Lit+Fp- phenotypes were obtained from
Lit+Fp+parents (e.g. matings 14, 15, 16). Fp+ was suppressed by modifier IF+
(matings 6B, 9, 10, 11, 12A). IF, did not inhibit Lit+ (mating 6B, Tables 3, 4).
Loci Lm and Cm (linea media and carina media)
The linea and carina media were pale lines on the mid dorsal head and pronotum
(Fig. 1, Table 5 ) . Both characters were often associated with each other. A positive
association with Ws'was recorded (x* = 22.52, P < 0.001 andxz = 18.17, P < 0.01
respectively, for 4 d.f.1. Crossovers were observed in most matings ofTable 5 and
linkage is suggested.
Matings 18B and 18C did not produce any Lm+Wo+or Cm+Wo+individuals,
indicating that Wo+inhibits Lm+ Cm+.
Single locus models could not explain frequencies observed in matings 6B, 7,
8B, 17B and 17C for Lm and matings 10 and 17C for Cm. Loci K and N inhibit
expression of Lm+ and Cm+.
Locus Z1 (zona lateralis)
The zona lateralis is a pale marking found on the lateral pronotum (Fig. 1).
Breeding experiments (Table 6) suggest a positive associationwith Wst(xz= 14.17,
Mak
18C
W-Fp+Wo+ x F F p - W o '
6
W m p - xm p +
WFp+ x m p 6A
6B
W F p +x m p m p - xm p +
8
8A
m p - xm p +
8B
m p - xm p +
m p - xdFp9
10
m p - xm p 11
m p - xm p m p +x m p +
12
12A
wh"Fp- x W F p 13
WFP-x w W - ~ p +
14
w p - xm p +
15
WwwFp- x W n p '
W F F p +x W m p +
15A
WFp+W"Fp16
W F p +F F p 17
17A
WFp' x W"Tp17B
W m p + x -p+
W F F p ' x WFp18
18B W""Fp-Wo+x WFp'Wo-
Mating Female
Phenotype
Possible genotype
2 Fp5 Fp+Wo-
-
3 Fp+Wo+
17 Fp-Wo+,
3 Fp+Wo+
5 Fp-Wo+.
-
2 Fp1 Fp-, 8 Fp+
-
5 Fp3 Fp-, 1 Fp+
1 Fp-
4 Fp-
2 Fp-
-
-
5 FpWo-
2 Fp+
2 Fp+
1 Fp'Wo-
-
6 Fp3 Fp+
1 Fp-. 2 Fp+
4 Fp-, 9 Fp+
4 Fp-, 2 Fp+
1 Fp+
-
-
2 Fp'
Stripemottled
4 Fp-, 1 Fp+
6 Fp-, 1 Fp+
2 Fp-, 1 Fp+
1 Fp1 Fp3 Fp-Wo-
-
-
2 Fp-, 1 Fp+
-
6 Fp-, 10Fp'
2Fp-, 3 Fp+
4 Fp-, 9 Fp'
7 Fp-, 1 Fp+
28 Fp-, 4 Fp+
20 Fp-, 4 Fp+
1 Fp-, 4 Fp+
4 Fp-
2Fp-.3Fp+
29 Fp-.
4 Fp+
3 Fp'
main
wing phenotypes of progeny
Mottled
6 Fp+
1 Fp-, 5 Fp'
1 Fp-, 4 Fp+
3 Fp-. 2 Fp+
3 Fp1 Fp-, 3 Fp+
-
-
2 Fp-, 3 Fp+
4 Fp+
-
Stripad
3 Fp-, 2 Fp+
1 Fp-, 2 Fp+
3 Fp-, 2 Fp+
3 Fp1 Fp-Wo-
4 Fp1 Fp+
-
6 Fp-, 1 Fp+
-
Light-mottled
Table 4. Crosses showing the inheritance ofthe Fascia postocularis (Fp).Crosses not listed did not have Fp+ in either parents or progeny. See
Table 2 for origins of parents
Table 5. Crosses showing the inheritance of the Lima media (Lm) and Carim media ( C m ) .Crosses not listed did not have Lm+ or Cm+ in
either parents or progeny. See Table 2 for origins of parents
P. GILL
256
P < 0.01)and crossovers were observed, suggesting linkage. Modifier locusJ was
postulated to account for the apparent deficiencyof Z1+ in matings 8,12,16,18 and
F, matings 8A and 16A. Wo+ appeared to suppress Zl+ (matings 18B, 18C),
although a singleWo+Zl+individual was observed in mating 18C. This may suggest
linkage ofJ with Wo,the observed anomaly being a recombinant u-Wo+).
DISCUSSION
Epistatic and linkage relationships
The following common associations were suggested :
-Striped pattern
CB, Wt Lm+, Cm+, Lit+, Fp+, Zl+
CB, PLm-, Cm-, Lit-, Lit-, Fp-, Z t -Mottled pattern
F o r f i o r R o r B l o r W W p Lm- , Cm-Plain, coloured pattern.
9
,
These associations may be aided by linkage of loci and maintained by
selection. The following epistatic interactions have been observed :
Wo+(wedgeless)suppressed striped patterncharacters Ws!ZP,Lm+ and Cm+.
L+ suppressed Pand Iy suppressed M"', producing plain-wing patterns.
.
M+ was shown to act as a s arate locus which roduced a mottled wingModifier loci Z, J, K, N an IF were associate with Lit, 21, Lm, Cm, an Fp,
respectively and caused inhibition of these characters. Alleles causing
repression were dominant.
7
B
F
Dominance relationships
The top dominant dorsal pronotum colour (locus C) was green followed by
purple and red; the position of black has not been determined but is probably
recessive to green; brown w a s the universal recessive; white was codominant with
purple and green but dominant to brown.
The coloured-plain wing (Wq was dominant to mottled (P)
and striped
( Wt), the two latter alleles being codominant. The plain wing ( W )
was recessive
to all other wingThe purple side pheno
was very rare in the wild. Sh was only
expressed in the presence o C and was dominant to brown sides (S?;FPL
(purple hind femora)was dominant to brown hind femora(F8).
Gill (1979)in a study of wild populations of C. b w m showed that over 80%
were brown, hence all the dominant alleles shown in this survey are rare in the
wild. Clarke (1964)gives a possible explanation for the occurrence of rare
dominants in animals.
Sansome 8c La Cour (1935)investigated the genetics of colour-patterns in the
related species C. purallelw. They claimed that linkage was not pronounced but
epistacy was common: Richards 8c Waloff (1954)suggest that predominantly
minor colour patterns were studied and question the validity of interpretation.
Further work on C.paraLZeh is required before comparisons with C.brunneus can
be made.
Nabours (19291, Nabours 8c Kingsley (19341, and Nabours et d. (1932)
investigated the inheritance of colour-patterns in grouse-locusts (Tettigidae),
finding control of patterns by epistasis and a series of closely linked genes.
?re,. TpnsPU
1SA
16
16A
17
18
18B
18C
IS
3
6
6A
6B
7
8
8A
12
13
14
xWwm021'
X W z I +
WF21+xwwmo21+
W21' xWPOZI- x W h a W21+x w-21WF21'xwPzI--wo+
xWZI+WoF z - W o +xFzl-Wo+
*Fa-
WPZI-
wzI+xwzIWn+xwwmon-
wzl- xwpzl-
wZl-xW%-
w21+
x--
W21+x wa+
W21+x wa-
wzl- xwPwlozl-aW F z l +x wzl+
Phenotype
Mating Female
Male
SZI+
4 a+
1 a+
Striped
w:wstzr+zl-x F F Z I - Z I W~W"ZI+ZI-J+J-x ~ W - Z I - Z I - J + J - wrwr~1-zlJ -J - x W ~ W ~ Z I +JZ+ JI -~ W Z I + Z I - J - J -x W ~ W - Z I - Z I - J + J ws'wzl+zI- x P w l l ~ z l - z l 2 21-, 4 21+
w . w z l - z I - x ws'wzl+zI+
6 21'
w ' w u z l - z l - x WS'W-Zl+ZI+
5 a+
WS'wuZl+ZI - x W S ' F Z l +ZI 5 zI+
WS'"''Zl+ZI- L+L-J-J - x F F Z I - Z I - L-L-J+ J - 221-, 1 a+
FWZI-ZI-J-I- x FwZl+ZI-J+JwW'Zl+ZI-T-T- x W-WZI-ZI-T+T421+
~ ' F Z l + Z IL-- L-J -J - x F W Z I - Z I - L + L-J+J- 7 ZI-, 2
wo- woF w z l - z I - w o + w o - x ws'wzI+zIw ' F z I - z I - w o + w o - x ws'FzI+zI-w o +w o - 421-, 1 ZI+
ws'w'zI+zIx w'w'zI+zIw'ws'zl+zI+
x W'w'zl-zl-
wFzl+zl-x w'ws'zI+zI-
w'ws'zl+zl- x W ' F z l - z l -
Possible genotype
4 a1 212218 2119 z1-, 1 21'
-
4 215 zl-
-
-
3 21+
2211 21+
421-, 1 zI+
1 a+
321-, 321+
9n+,
421421-, 221+
1 21-, 221+
121-,221+
2 a+
721321-,421+
1 ZI321-
-
3 ZI+
11 21121-,421+
4211 21-, 31 21'
17 21-, 3
16 21421-, 1 ZI+
421-, 1 21+
-
Wing phenotypes of progeny
Mottled
Stripemottled
Plain
zl-
1021-, 1 zl+
321-, 221+
3211
-
5 ZI-
421-
-
Light-mottled
Table 6. Crosses showing the inheritance of the @
, uz lateralis ( Z l ) .Crosses not listed did not have Z1+ in either parents or progeny. See
Table 2 for origins of parents
P. GILL
258
Colour changes in Orthoptera
Physiological changes in colours of insects are uncommon but do occur in
Orthoptera. In Carawius (Phasmida)changes in light cause individuals to become
brown in the daytime and black at night due to movement of pigment in the
epiderman cells (Dupont-Rabbe, 1957 1. In the Australian grasshopper, Kosciuscolu
tristis, Key & Day (1954) showed that above 25OC males were blue and below 15OC
they were black. These changes were probably associated with thermoregulatory
functions since black insects absorb more heat than paler ones.
Morphological colour changes occur in tropical grasshoppers and locusts
(Uvarov, 1966). Black grasshoppers are common in regions recently affected by
bush fires in Africa and some individuals of Phorenula wemerianu change from
grey to coal black in two days. Such changes only occur in bright sunlight,
however.
Temperature may be important in pigment development in locusts (Goodwin,
1952); crowding also affects colour-patterns (Stower, 1959). Colour changes are
often associated with aging and maturation (Burtt & Uvarov, 1944).
Darkening of C. brunneus colours were observed in recently emerged adults and
was especially noticeable with the green pattern. Purple sided individuals
generally became paler, however.
In C%!P heterozygotes, nymphs and recently emerged adults are neither green
CBSB
nor purple, but an intermediate dark brown colour, but after a few days, the
green colour develops'and becomes clearly visible, albeit somewhat darker than
that which is usually observed. Dominance of the green genotype seems to be due
to its greater activity in laying down pigment in the adult in this case. The purple
sides remain unchanged. This phenotype has not been reported in the wild.
Adaptive signiicance of colour-pattern variation
There is little doubt that colour-patterns can influence predatory behaviour
(Clarke, 1962) and that redators can alter morph fiequencies (Cain8c Sheppard,
1954). Birds and lizar s are known to take grasshoppers (Richards & Waloff,
B
1954).
Chorthippus brunneus is found in a wide variety of habitats, ranging from
meadow to sparsely covered wasteland. Gill (1979) suggested that morph
frequency differences occurred between different types of habitat. Striped forewings ( W'),lineu media (Lm+)
and carinu media (Cm+)predominated in well-covered
meadows. These characters may act as camouflage against a background of long
grass; conversely, such patterns may be conspicuous against a background of
bare earth and rocks of wasteland. Characters such as mottled fore-wing(Wh")
and wedgeless ( Wo+ suppresses striped patterns) may be advantageous against
such backgrounds, however.
There are several rare colour pheno es (locus C)-green, purple, redbrown, black and white-all are genetical y dominant to the common brown
genotype (0.
Some phenotypes are extremely rare. The urple-sided variety
(9")
was only observed in two out of 42 populations (P.Gilf Unpubl. data) and
the green sided variety ( S G ) reported by Ragge (1965) was not observed at all.
Each colour may act as camouflage against the appropriate background (Gill,
1979), e.g. white against hay or straw, green against living vegetation, brown or
?)
GENETICS OF COLOUR-PATTERNS IN C. ERUNNEUS
259
black against earth. British species which live in lush vegetation e.g. Omocestus
uiridulus, C. parallelus have high frequencies of green phenotypes (Ragge, 1965 ;
Richards 8c Waloff, 1954). Petersen 8c Treherne (1949) showed that green morphs
of 0. uiridu/us were more frequent in green habitats compared with dry, brown
looking habitats.
In conclusion, the expression of major colour-patterns in C. brunneus is under
genetic control by a large number of loci and involves linkage and epistacy.
Minor variations in colours or wing patterns are probably age-dependent.
ACKNOWLEDGEMENTS
This work was supported by a research grant and fellowship from SRC. I am
grateful to Professor B. Clarke for his useful comments and criticism of an earlier
manuscript.
REFERENCES
BUR=, E. D. & UVAROV, B. P., (1944). Changes in wing pigmentation during the adult life of Acrididae
(Orthoptera). Proceedings ofthe Royal Entomological Society ofLondon (A) 19: 1-8.
CAIN. A. J. & SHEPPARD, P. M., (1954). Natural Selection in Cepaea. Genelics, 3 9 : 89-11.
CLARKE, B., ( 1962). Balanced polymorphism and the diversity of sympatric species. Acblicafions. Systemaiics
Association, 4 : 47-70.
CLARKE, B., ( 1964). Frequency-dependent selection for the dominance of rare polymorphic genes. Evolution,
18: 364-369.
DUPONT-RABBE, M., (1957). Les mkcanismes de I’adaptation chromatique cha les insectes. Archives de
zoologie expirimentale et g h i r a k , 9 4 : 61-294.
GILL, P. D., (1979). Colour-pattern variation in relation to habitat in the grasshopper Chwfhippus h n m
(Thunberg). Ecological Entomology, 4 : 249-251.
GILL, P., (1981). Enzyme variation in the grasshopper Chthippus brunnew (Thunberg). BiologicalJournal ofthe
Linnean Society, 1 5 : 247-258.
GOODWIN, T. W., (1952). The biochemistry of locust pigmentation. Biological Reviews, 27: 439-460.
KELLY-STEBBINGS, A. F. & HEWIlT, G. M., (1972). The laboratory breeding of British Comphocerine
grasshoppers (Acrididae: Orthoptera). Am’da, 1: 232-245.
KEY, K. H. L. & DAY, M. F., (1954). A temperature-controlled physiological colour response in the
grasshopper Kosciuscola trislis Sjost (Orthoptera: Acrididae). Australian Journal of Zoology, 2: 509-359.
KORNERUP, A. & WANSCHER, J. H., (1963). Methum Handbook ofColour. London: Methuen.
NABOURS, R. K. (1929). The genetics of the Tettigidae (Tetriginae). Bibliography of Genetics, 5 , 27-104.
NABOURS, R. K. & KINGSLEY, L. L., (1934). The operations o f a lethal factor in ApPofettix cutycephalus (grouse
locusts). Gaelics, 19: 525-328.
NABOURS, R. K., LARSON, I. & HARTWIG, N., (1932). Inheritance of colour patterns in the grouse locust
Actydum arenosum Burmeister (Tettigidae). Genetics, 18: 159-1 7 1.
PETERSEN, B. & TREHERNE, J. E., (1949). On the distribution of colour forms in Scandinavian Omoceslus
uiridulus L. Oihos, I : 175-185.
RAGGE, D. R. (1965). Grtushoppers, Crickets and Cockroaches ofthe Britirh Isles. London: Warne.
RICHARDS, 0. W. & WALOFF, N., (1954). Studies on the biology and population dynamics of British
grasshoppers. Anti-lonut Bulletin, 17: 1-182.
SANSOME, F. W. & La COUR, L., (1955). The genetics of grasshoppers: Chthip/nu parallelus. Journal of
Genetics, 30: 415-422.
STOWER, W. J., (1959). The colour patterns of hoppers of the desert locust (Schidocercagregaria Forskal). Antilocust Bulletin, 32: 1-75.
UVAROV, 8. P., (1966). Grasshoppers and Lonuts. Cambridge: Cambridge University Press.