<>/ ffit1 l.inni'nn \<xiclY \ l ' W O i . >9 .V27 , V M . \ \ i i h î ligures
A decline of melanism in the peppered moth
Biston betularia in The Netherlands
PAUL M . B R A K L F I K L n
Section oj Evolutionary Dio/ngr, Department <>J Population lîiologv, l'nnrrMty of I.eitlen.
I4a, 2313 £1 I.mini. I In Netherlands
Mi I. l l l l i f o r m s ni t i n peppered mol II lit \lnn hrluliilln w e r e we'll e s t a b l i s h e d i l l I hi \ el hi I l a n d s In i h r end of i h r I ' l l l i i r u n n y , i n d r r d i l » I H M n t m i l s of i h r l i l a c k inihimniin lonn i n I H ( > 7 .in i i n h . i l n n i l 20 years l . i i r r i l l . i n in I'.n^l.ind A n . i U s i s öl i \
prriod ol srvrr.il y i . n s In 14111111111; i n 1'ld'l sin 70",, i n must n l ' i h i i i u i n l r v w h i r r r p i p h y t r u .ill pollution. I h r p.ill Iv/uiii .nid i h r l l n r r l l l r i | i i r i u 1 r s ( ) n l \ i n l l n r s l r r n i r n i i i l h .nul
eruive sampling data collected b) H | I , r m p k < im .\
w s i l l . u ifjthtuiiinil \ \ . i s .11 .1 l i r < ] ! i i i n \ nl a l u m ! liO i n ill i n n 111 l u s u i l U i i s H I H n dm ed dm lo I hi i Hi i Is of i i n n u d i . l l r insuiana forms w r i t c.u h .il s i m i l a r . low c i i i l l i r.isl n l I I n N r l h i ' r l . i i i d ' . w lli'l'i r p i p l i M r l l n i . i s u r i r n« her w . l s iinhiiiiiiini a t a lower l l r i ] l l r i n \ o l Irss i h a n H I S.nnplrs l o l l e i t r d l l o n i S I M M loi . d u n s in I ' I K K show t h a i inrlnmnriii h.is d i . n n . i t i i a l l s dei lined lo a l n i | u i i i i v ol less i h a n 10 , , In t o n t r . i s t lo Km»l,nid. t h e fully blai k lonn is hrini; r r p l a i rd not m i l s In IV/HIH I n n also In the d.n krsi of i h r HUM^afifl pheiiolypes I he d e c l i n e in m e l a n i s m i omi itles w i l h a period of decreasing l e x e l s ot s u l l ) l n l l d l o M i l e and ol i n i l e a s n i i , ' spines d l s e r s i l s ol l u l l e n s on l u e s
K l \ \ \ O R D S lin/un hiluliiiin p e p p e n d m o t h i i i d n s t i i . i l m e l a n i s m i x o h n i o n p o K i n o i p l n s i n n . H m . i l si lei l i o n .111 p o l l u t i o n i p i p l n t i s
CON I I . M S
I n t r o d u c t i o n
Snis'eys ol finlon ln'hilinin i n I he Ni I In i l a n d s
Hie 1 9 t h i r n t u r y 'Î2tt I ' M , ' ) lo 1973 i-'K 1988 129 I )|SI I I S S I 0 1 1 Acknowledgementi R r l r i r i i i r s Ü Ü t 1\ I ROD! ( I I O N
Sitidics ol' i n d u s t r i a l melanism have gained new i m p e t u s in recent years \ \ i t h the discovery of f u r t h e r evolutionary chance occurrint; in the form of declines in t h e frequency of mchmic forms of the peppered moth liislon hclulana and the i\vo-s|)ot ladybird beetle Ada/in bipiuictatn in some urban environments in Britain (Clarke, Mani & Wynne, 1985; (look. Mam' & Yarley, 1986; Howled c\-Majerus, 1987; Creed, 1971; Brakefield & Lees, 1987). Such phenomena provide excellent opportunities for experimental analyses of n a t u r a l selection involving both visual and non-visual elfei Is of t h e major genes controlling the m c l a n i i
397
328 l' M. H R A K I . K I K I . I )
polymorphisms. Insights from such studies will be critical to improving our rather rudimentary understanding of this classic example of the spread of adaptive phenotypes under the influence of natural selection (see Brakefield, 1987; Mani, 1990). Although both the moth and ladybird appear to be responding to decreases in air pollution, there are clearly important differences in the underlying mechanisms (see Brakefield & Lees, 1987; Brakefield, 1987; Liebert & Brakefield, 1987).
The present study provides a basic description of a recent dec l i n e in the frequency of the black carbonaria form of H. helularia in The Netherlands. Although this phenomenon tends to parallel the changes in B r i t a i n there are at t h e same t i m e some i n t e r e s t i n g differences in detail. Unfortunately, u n l i k e the monitoring studies of B. b e lul aria at Caldy near Liverpool (Clarke el, a/., 1985) and o f / I . bipunctala in Birmingham (Creed, 1971; Brakefield & Lees, 1987), d a t a points are only a v a i l a b l e for the present-day and for some I f ) to 20 generations (years) earlier.
SI K V I . Y S O I / ( A / C M ni:ll I.MU.\ l,\ I I I I ' , N K I ' H K R I . A N D S The 19lh century
The first recorded observation of a black peppered moth in England was made in 1848 in M a n c h e s t e r (see Cook, 1981). The f i r s t record from The N e t h e r l a n d s is not m u c h later (see Lempke, 1970). A m a t i n g pair of black moths was found on an elm tree at Breda in N o o r d - B r a b a n t in 1867 (Heylacrts, 1870). The p a i r i n g is depicted in a p l a t e by S. van Vollenhoven. The discovery of a mating pair suggests t h a t even by 1867 a dominant carbonaria allele was present at a s u b s t a n t i a l frequency in certain populations. In any case inspection o f ' m a t e r i a l in the Zoological Museum of Amsterdam shows that by the end of the 19th century melanic forms of II. helularia were well established in the greater part of The Netherlands. These melanic forms i n c l u d e d not only carhonaria but each ol the three main phcnotypcs recogni/cd within the ( l a s s of i n t e r m e d i a t e insttlaria melanics. These phcnotypes arc all determined by a series of alleles at the
carbonaria locus. Lempke (1970) states t h a t the earliest specimens of the four
forms (see below) in the /oological Museum of Amsterdam are dated 1871, 189"), 1888 and 1884 (in order of increasing melani/ation).
to nm
B. J. L e m p k e w o r k i n g in the 1960s recogni/ed the v a l u e of a survey of
K. helularia throughout The Netherlands. Entomologists were enlisted to send
samples o b t a i n e d in light traps to him for scoring and synthesis. Moths were scored after consultation with H . B . I ) . Kettlewell and study of Keith-well's collection. Lernpke d i s t i n g u i s h e d five phenotypes: fully-black carbonaria] light
lypica; dark imularia ( I , ) , very dark with very light, or light specking; medium i ii MI I ana (I2) w i t h s u b s t a n t i a l speckling; pale ///Mi/aria ( I , ) , more black scaling
D l . C I . I M N C , M l . I . \ \ I S \ 1 l \ / ; / s / 0 \ l \ H O I I \ M ) ( 2 9
l M U I I. Percentage l i c q u c i u v <>l the h \ c major non-raelan« .nul melani< phenotypea <>l the
peppeied m o l l i Un/un hiliiliiini in pooled samples obi.nncd in ten D n l d i I V m i i u c s 1>\ I V ) . l . e m p k e l i o i n 1969 lo 1973 (sec t e x t ) . T o t a l sample si/es a i e .ilso i ; i \ r n
]'( n c t i l . i i > r [ i c q u r i K \
I d i a l s.niiplr
Province Ivlnni in\iil. ! until. 2 intiil ,'i' carlwminu si/(
1 i n s K i i u l Drenthe ( )\ ( 1 1|SS( 1 Noord-Holl. nid Gdderland Utrecht / m i l l l d l l . l l l d Noord-Brabanl /i 1 1. n u l l . i n i h u i t; 19.1 16.2 13.9 12 J 7.0 9.0 4.3 3.7 12.1 2.3 ld 20 9 10 8 10 7 :i 18 4 3 9 G 1 5 2 8 0 2 5 16.3 17.4 '1 i 88 17.4 1 1 1 9 9 10.4 22.7 10 8 14.7 4.7 J 8 - 1 (> 1 ( 7.9 9.8 7.3 ld ,'! 9.1 9 h 3.6 I'M 0.7 86 8.8 HO 2.3 377 9 1 328 7.8 2:ï<i 0.7 232 2.1 297 ! 7 9 ( , i , J ' » 17(11)
(1973: table 6.1). Lcmpke most gencroush made the complete d a t a set a v a i l a b l e lor the present analysis.
A total of 4486 male B. belularia were oblained from H I localities. H o w e \ c r , (VI s i t e s yielded less t h a n ten m o t h s and only 27 samples \\ere of' 10 or more moths. I he samples provide a fairly thorough coverage of the c o u n t r y , only the e x t r e m e north ( t h e Province of Groningen) being unrepresented. P r e l i m i i i a i \ examination of the d a t a indicated broad regions of s i m i l a r morph frequencies.
Chi-square (x2) heterogeneity tests were applied to the (requeue) d.ila for the
localities gr'ouped by Province or by contiguous groups of Proxinccs. The t e s t s provided s i m i l a r results when the phenoUpcs \\crc grouped e i t h e r b\ (vfuca and all melanica or by typica:insulana:carbonaria. The l.irger samples from most of the i n d i v i d u a l Provinces are homogeneous (f>0.05). This included Limburg in the s o u t h - e a s t , the Province w i t h the highest frequencies of /tn/xnitnin ,uid the only one w i t h more t h a n two or three separate samples (jf «48.58, d.f. = 3(i and ten sites, /'>().05). 'I'he data pooled by Province are given in Table 1. Each of the l i v e phenotypes was collected t h r o u g h o u t the c o u n t r y . 'I'he h'/nca form and each of the three iiiM/ltiriti phenol\pes were of roughU s i m i l a r abundance. I he geographical v a r i a b i l i t y in the frequency of ctirhonnria is illustrated iu Fig. 1 together w i t h .111 i n d i c a t i o n of the p a t t e r n of' ^ homogeneity across Provinces. Most of The N e t h e r l a n d s was c h a r a c t c r i / c d b\ high fre(|iiencies of carlniiKina of about (i() or 70°,,. Hovvexer, Friesland and D r e n t h e in the n o r t h , and /eeland in the extreme south-west had louer frequencies of around -10°,,.
1988
330 l' M M R A K I . I I I . l D
1969-1973
carbonana
Kiicurc I M i l ) ) nl I In1 N e l l l e i l , n i d s showni!* i h r frequency n l ' l l i c inilmniiriil l i m n nl Itnlini hrliiliiilii i l l i l i < pi nod l'(li') in 1973 ' + ) . Broken l i n e s iiow i h c borders bel ween i l i e D u n h I ' r o v i n i e s . two ol w l n i h .m n , l i n e d Shadms> i n d u aies die p a t t e r n ol homogeneity in morph-frequencid .11 ross I ' n i M i u i s si i i i \l. d , H , i ni I! ) l . e i n p k e . \o samples were « o l l n l i d i n t h e a n . i s i n d u aled by q u e s t i o n m a r k s 1 lie inset m a p shows i h e e p i p h y l l i v e l v e t , i l i o n i n l i n I ' H i O s w i t h "deserts" dulled.
transitional /one in a li/lt' w i t h poor lo l o i . t l k s u b l i m i n a l \ i t ; e l a t l o u . n o r m a l 01 h i x u n a n l areas
linli/iff! I ..11151 ' t o w n s and mam i n d i l s l n . i l an as ale m b l a i k I liree < Hies n< al u l i l i h s a m p l e s were
o h l a m e d m I98H a n i n d u a t e d A A l i i s l e r d a l l i . I . . I.eiden a n d R . R o t l c r d a m : a l l e r B . i l k m . i n . I ' l l i ' l
I ' A H I K 2. N u m b e r s o f t h r five major t i o t i - i i i c h i t i n and melanii p h e n n l y p c s of t h e peppered moth
lii\l(in hilnliniti in s a m p l e s obi.lined I'rotn the i n d i c i i t e d l o c a l i l i e s in I ' l l i f ! I he I n s l t h r e e l o e a l i t i e s
are in the vicinity of'Leiden and the next two are pist to t h e west of R o t t e r d a m (see l''ii;. 1)
D K C I . I N I M . M l I \ \ l s \ l I N / ( / s / ( M I N HOI l \ \ D 331
l.icbcrl. Il sliould, however, he recogni/cd t l i . i t the phenol) pes intergrade and i h n s t h e r e is i n e v i t a b l y some s u b j e e t i v i t y in a s s i g n i n g e e r t a i n i n d i v i d u a l s to p a r t i c u l a r p h e n o l ) pes. This is prob.ibh c s p e c i a l l ) so lor the b o u n d a r i e s b e t w e e n
hfniti and niMtlaria I and b e t w e e n iii\iilariti ,V and i/ii/miitinii see also Lees & Creed,
1977; (Harke, 1979). My own experience is t h a t t h e bod) colouration is critical
34%
53% 1986
1969-fyp/co msul. carb.
l i g u r e > Comparison ul m o r p h II r < | i n lu le s in I ' l l ) ' ) I ' I 7 ! l o u e î - n i i i s l h i s i < u > r . ! t i i s \ \ n l i ||IOM ol'
I'liiii l lu earlier samplet are thaw pooled for each of two Dutch Province! M-C 111; 1 I h c - l . n c i
s . u n p l c s I K I I I I l l u s.iMH l'ni\ l i n e ' s .ire cilhcr lor i m l u i d n . i l M U A or ponldt loi neighbouring l o i . i l i l i c s iscc I . i l i l i - 21 I V r c c i n . i n c ' frequenda are indicated foi i l n i l m < mm phs \ho\\ nn> M i l i s i . i n i i . i l i h.mm•>.
332 l' M . BK A K 1,1 11.1,1)
in the former case, and the presence or absence of a more or less complete ring of light white speckling on the upper hindwing, in the latter.
The frequency data for the samples collected in 1988 are given in Table 2. Figure 2 illustrates the dramatic changes which have occurred in less than 20 generations. In the area of Zuid-Holland and Noord-Holland the frequency of
carbonaria has declined from about 70% to less than 10%. Apparently it is being
replaced not only by typica but also by the darkest form of insularia. The two paler forms of insularia have not changed substantially in frequency. There has also been a dramatic decline in carbonaria in Friesland but from initially lower levels.
DISCUSSION
The inset diagram in Fig. 1 shows that there was some spatial correspondence in the late 1960s between melanism in R.belularia in The Netherlands and the growth of epiphytic lichen communities on trees (Barkman, 1969; see also map for 1972 given by de Wit, 1983). The only two regions w i t h low frequencies ( < 4 0 % ) of carbonaria were those in the north and extreme south-west with comparatively luxuriant lichen communities. The rest of t h e country which includes the major industrial conurbations was characterized by high frequencies
of carbonaria of around 60 or 70% and by impoverished epiphyte growth (Fig. 1 )
and high levels of air pollution, especially s u l p h u r dioxide (reports of the Dutch Rijksinstituut v. Volksgezondheid). Thus d u r i n g this period R. betularia seems to have displayed classic industrial melanism with a correlation between air
250-1965 1970 1975 1980
I
I
Elm Willow Poplar Lime
I
-1984 -1973
Total
Kigurc !i. A. A v e r a g e concentration of'sulphur dioxide recorded monthly at Schiedam in /.uid-lloll.ind from 1965 to 1983; broken line shows ruiming annual mean. B, Mean number of'species of
epiphytic lichens re< ordcd at numerous siles in /uid-Holland on d i f f e r e n t tree species in the years
DKCUNING MLLAMSM I N /!/\/l>\ I N HOLLAND 333 pollution and m c l a n i c frequencies. However, the apparent!) early establishment
of the melanism in The Netherlands is noteworthy since d i i f i i i » ' the mid- to l a t e n i n e t e e n t h c e n t u r y , industrialization was m u c h less i n t e n s i v e and more locali/ed t h a n i n n o r t h e r n E n g l a n d .
The frequency ol\ carbonaria lias declined q u i t e d r a m a t i c a l l y in t h e last 20 or so years. This appears to p a r a l l e l the c h a n g e in mam p o p u l a t i o n s in n o r t h e r n
England and which is best d o c u m e n t e d at Caldy near Liverpool ( C l a r k e <•/ u / . .
1985) where carbonaria has declined r a p i d l y from about 90",, to 40",, since 1970. Cook f / < 7 / . (1986) show t h a t t h i s change is consistent w i t h a more or less c o n s t a n t selective d i s a d v a n t a g e to carbonaria of about 12",, compared to the earlier period. However, at Caldy carbonaria is being replaced largely by I_Y/HCII; wsularia increasing from below 1",, up to only about •!",,, w i t h each of the t h r e e classes being represented (Mani, 1990; C. A. Clarke, personal c o m m u n i c a t i o n ) . This suggests t h a t a more complex change in the r e l a t i v e Illnesses ol' the various genotypes is occurring in The N e t h e r l a n d s where both (vpica and ( d a r k e r )
inxularia are increasing at the expense o(' carhonana.
Models of the decline in carbonaria at Caldy have shown that it is closely correlated with a reduction of sulphur dioxide in the locality ( M a n i , 1990). Fig 3A shows a typical d a t a sel i l l u s t r a t i n g the progressive decline in levels of sulphur dioxide which has occurred since the early 1970s in the Province of Zuid-Holland and elsewhere in The Netherlands. Although s u l p h u r dioxide is not the only s i g n i f i c a n t factor influencing changes in t h e epiphytic lichen communities in The Netherlands (de Wit, 1983) there is clearly a correlated increase in lichen species diversity on a v a r i e t y o l ' t r e e species in Z u i d - H o l l a n d (Fig. 3B). Small colonies of foliose lichens now occur on the t r u n k s and upper surface of branches in trees in ciliés in this area. This may be an important factor, together with more general changes in bark c o l o u r a t i o n , i n f l u e n c i n g relative crypsis in Bi.üon moths (see discussion in Liebert & Brakelield, 1987).
Mani (1990) in a modelling approach to examining changes in fitness in the population at Caldy assumes t h a t hiMilaria suffers less loss of fitness with reduction in air pollution than carbonaria. The frequency data from The N e t h e r l a n d s suggest t h a t the darker insulana phenolypes may indeed experience less loss of fitness there a n d , moreover, t h a t they may have s i m i l a r fitness to the
typica form. F u t u r e experimental analyses of moth crypsis will investigate the
possibility that changes in the a v a i l a b l e resting backgrounds for B. belitlaria in trees in central Holland have led to a switch from a bias towards those giving
carbonaria the closest background-matching to a mixture of some favouring
darker insnlaria and some, Ivpicti.
ACKNOWLEDGEMENTS
My great debt to Dhr B. J. Lcmpke for m a k i n g his d a t a and knowledge freely a v a i l a b l e to me w i l l be obvious to all readers. I also t h a n k all the D u t c h entomologists who contributed to his survey. I am also most grateful to Tony Liebert for breeding the stocks used for assembling and for v a l u a b l e assistance with the l i e l d u o r k and developing my scoring system. I t h a n k S t e p h a n i e M e r e d i t h and Frans v. Eysinga for t h e i r h e l p in c o l l e c t i n g in A m s t e r d a m and
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