Heredity 54 (1985) 251—254 The Genetical Society of Great Britain Received 27 September 1984

Non-visual differences between colour morphs of the polymorphic snail arbustorum

A. H. AbdeIRehim*. Department of Zoology, University of Manchester, S. E. R. Bailey and Manchester M13 9PL, England. L. M. Cook

Brown shelled morphs of Ariantaarbustorum aremore frequent in shaded woodland than in open, sunnier habitats. This is thought to be the result of selective visual predation (Parkin, 1971). Yellow shelled morphs have a higher metabolic rate than browns, especially at high temperatures, and remain more exposed to sunlight. These non-visual differences in metabolism and behaviour will offset differences in radiant heat gain which result from the two shell colours in open habitats. Differences in heat gain will seldom occur in shaded habitats. The non-visual differences therefore appear to adjust for differences in energy gain caused by shell colour, rather than to act as component forces generating the polymorphism. They therefore do not have a balancing effect.

INTRODUCTION scored. On the other hand, visual polymorphisms in a wide range of genera in a variety of families Thecauses of polymorphisms in land molluscs are correlated with living in heterogeneous foliage continue to be discussed. Some authors argue that habitats (Clarke, Arthur, Horsley and Parkin, selection is relatively unimportant. For example, 1978), while in other types of habitat are the large scale patterns of isozyme frequencies in more likely to be monomorphic. This suggests that Cepaea nemoralis studied by Ochman eta!. (1983) the effects on fitness act through the properties of are interpreted as due to accumulation of genetic the visual phenotypes themselves. differences in small populations through adaptive An explanation depending only on visual response, genetic drift or both, followed by appearance is that predation operates in a expansion and secondary contact. Moreover, frequency-dependent manner to conserve variety because no relationships of allele frequencies with (see Clarke eta!., 1978). This would be most likely environmental variation have been found, it seems to be effective when the morphs are very distinct unlikely that adaptation to local environments has from each other in appearance, as in Cepaea. been involved (Selander and Ochman, 1983). However, differences in colour also affect the Agreement has not been reached on the factors amount of energy of certain wavelengths received likely to maintain visual polymorphisms in this by the within the shell, and it is possible and other species (e.g., Jones, Leith and Rawlings, that polymorphisms may arise as a result of a 1977). If selection is claimed to be involved it is balance of crypsis and of the differences in net always possible to argue that the fitness differences energy gain which are a necessary concomittant of are due to otherwise undetected loci linked to those the visual differences. The experiments discussed controlling the visual phenotypes. In that case it here were undertaken to look for possible balanc- would be impossible to arrive at an explanation ing interactions between visual and non-visual related to the properties of the morphs which are properties of a pair of distinct visual morphs. The experimental design and full details of the outcome * Presentaddress: Department of Zoology, AI-Azhar Univer- are given elsewhere (Abdel-Rehim, 1983a, b, sity, Nasr City, Cairo, Egypt. 1984a, b). 252 A. H. ABDEL-REHIM, S. E. R. BAILEY AND L. M. COOK

MATERIALS AND METHODS Land snails have relatively poor physiological homeostatic ability, and respond readily to change Thesnail Ariantaarbustorum ispolymorphic for in physical conditions (Steigen, 1979). Differences shell colour over much of its range. The morphs in response between the morphs are likely to be have a pigmented shell, usually with a single band, small in comparison with the overall changes. The or an unpigmented shell, usually bandless or intention was therefore to look for interactions hyalozonate handed. Coupled with the yellow pen- between morph and one or other of the physical stracum they appear brown or yellow (Cook and factors which were varied. Significant interactions King, 1966). It is known that browns are at a higher would indicate that the morphs respond differently frequency in woodland than in open habitats in a to the change and thus differ itt adaptation ability. given area, and there is evidence of selective preda- Higher order interactions may also he meaningful, tion (Parkin, 1971). Yellows are on average at but they are difficult to interpret, and are therefore higher frequencies in humid regions than in dry not discussed. ones, indicating that relative fitness is correlated in some way with climate (Parkin, 1972, Cain, Cameron and Parkin, 1969). The species is there- RESULTS fore a good one in which to examine the relation between the visual and the non-visual attributes Theresults are shown in table 1, which gives the of the morphs as a step towards building up a significance of the main effects and the first order picture of how the polymorphism is maintained. interactions with colour in the five experiments. A The material was collected at intervals over five factor which was not tested is indicated by a dash. years from a single location in Miller's Dale, Der- There is a main effect of shell colour only with byshire (National Grid Reference SK 133728). We respect to metabolic rate, yellow individuals hav- do not know whether the results are applicable to ing a very significantly higher metabolic rate than other populations, but the procedure used browns. There is also a significant interaction of minimises the possibility of effects arising from colour and environmental temperature. Tem- inter-population variation. Many studies of poly- perature was varied from 5°C to 30°C in steps of morphic snails have been criticised on grounds of 5°C. There is a negligible difference in metabolic weakness arising from this source (Clarke et a!., rate between colours at 5 and 10°C, but a progress- 1978). A series of five independent factorial experi- ive divergence at higher temperatures (table 2(a)). ments was carried out, in which (a) nocturnal Yellow snails also eat less food than browns at activity, (b) food consumption, (c) assimilation 5°C and more at 20°C. Although the pairwise efficiency, (d) metabolic rate and (e) mortality were comparisons at each temperature are in no case measured in juveniles and adults of the two significant (table 2(h)), the result is a significant phenotypes at a range of adaptation temperatures, interaction between morph and temperature with periods of acclimatisation and experimental tem- respect to food consumption (P<004). With peratures and humidities. regard to assimilation efficiency there is an interac-

Table 1Summaryof fivefactorial experiments, showing the significance of the effect of varying the factor at the left on response as measured by the variable at the top

Variable measured Nocturnal Food Assimilation Metabolic Mortality Source of variation activity consumption efficiency rate rate

Adaptationtemperature (T) <0'OOI <002 os. <0'OOI is. Relative humidity (H) <0001 <<0001 <<0001 <<0001 n's. Age (A) n.s. <<0'OOl os. — <<0001 Environmentaltemperature (El — — <0'OOl <<0•OOl Period of acclimatisation ( W) <0001 <000l <0'OOl Phenotypic shell colour (C') OS. n.s. n.s. <<0'OOI 0.5. C x T n.s. <0•04 os. n.s. n's. C x H n.s. n .s. 0.5. n.s. n.s. fxA n's. Ii .S. <0003 C'xE — <<0001 n.s. Cx W n.s. n.s. 11.5. — n.s. DIFFERENCES BETWEEN COLOUR MORPHS 253 tion between stage of development and morph colours in open vegetation. The difference in (P

(c) Assimilation efficiency ABDEL-REHJM, A. H. 1983a.Ph.D. Thesis, University of mean assimilation (%) Manchester. Stage I Brown Yellow ABDEL-REHIM.A. H. 19836.Differences in habitat selection by different morphs of the snail Arianta arbustorum. Biol. J. Juvenile 0-07 96-1 98-5 Linn. Soc., 20, 185-193. Adult —1-86 97-1 96-2 ABDEL.REHIM,A. H.l984a. The effects of temperature and humidity on the nocturnal activity of different shell colour morphs of the Arianta arbustorum. Biol. I Linn. Soc., 20,385-395. ABDEL.REHIM,A. H. 1984b.Metabolic adaptation in the poly- CO N CLU SIO N morphic land snail Arianta arbustorum. J. mall. Stud. 50, 96-103. The two morphs perform very similarly, except CAIN,A. J., CAMERON, R. A. D. AND PARKIN, I). T. 1969. that metabolic rate is higher in yellows than in Ecologyand variation of some helicid snails in northern browns. At higher temperatures yellows have a Scotland. Proc. rnalac. Soc. Land., 38, 269-299. CLARKE,B. C., ARTHUR, W., HORSLEY, t). T. AND PARKIN, D. higher food consumption and a lower assimilation T.1978. Genetic variation and natural selection in pulmon- efficiency, while as temperature drops this effect ate molluscs. In Fretter, V. and Peake, J. (eds.) Pulmonates, is reduced and may reverse. Abdel-Rehim (1983b) vol. 2A. Academic Press, New York. has shown that in the wild, yellow snails from the COOK, L. M. AND KING, J. M. u. 1966. Some data on the genetics area studied remained more exposed to light than of shell-character polymorphism in the snail Arianta arbus- torum. Genetics, 53, 415-425. browns. During three days observation in May they HEATH, D. ..1975.Colour, sunlight and internal temperature were more active than browns on the surface of in the land snail Cepaea nemoralis (L.). Oecologia, Berlin, vegetation in late afternoon. There is therefore a 19, 29—38. behavioural difference between the morphs with JONES, J. S. 1973. Ecological genetics and natural selection in which the metabolic difference will interact. It is molluscs. Science, 182, 546—552. JONES, J. S., LEITH, B. H. AND RAWLINGS, i'.1977.Polymorph- known that visual predation acts on this species, ism in Cepaea: a problem with too many solutions? Ann. favouring dark colours in wooded areas and pale Rev. Ecol. Syst., 8, l09-l43. 254 A. H. ABDEL-REHIM, S. E. R. BAILEY AND L. M. COOK

O('HMAN, H, JONES, J. S. AN!) SLLANDIR, R. K. 1983. (urreflt Topics in Biological and Medical Research. 10, 93- Molecular area effects in Cepaea. Proc. Nat!. Acad. Sci., 123. USA, 80, 4189-4193. siE!c;LN, A.L. 1979. Temperature effects on energy metabolism PARK!N,D. !.1971. Visual selection in the land snail Arianta in banded and unbanded morphs of the snail Cepaea arhu,ctorum. Heredity, 26, 35-47. hortensis Mull. Oecologia, Berlin, 4!, 163—173. PARKIN,D. T. 1972.Climatic selction in the land snail Arianta TILLING, S. M. 1983. An experimental investigation of the arbustorum in Derbyshire, England. Heredity, 28, 49-56. behaviour and mortality of artificial and natural morphs SELANDER,R. K. AN!) O('IIMAN. H. 1983.The genetic structure of Cepaea nemoralis (L.). Rio!. J. Linn. Soc., 19, 35-50. of populations as illustrated by molluscs. In Isozytnes: