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INHERITANCE OF THREEDORSAL COLOR/PATTERNMORPHS IN SOME TURKISHPHILAENUS SPUMARIUS(HOMOPTERA: CERCOPIDAE)POPULATIONSSelcuk Yurtsever aa School of Pure & Applied Biology, College ofCardiff, University of Wales , Cardiff , CF1 3TL , UKPublished online: 30 Apr 2013.

To cite this article: Selcuk Yurtsever (1999) INHERITANCE OF THREE DORSALCOLOR/PATTERN MORPHS IN SOME TURKISH PHILAENUS SPUMARIUS (HOMOPTERA:CERCOPIDAE) POPULATIONS, Israel Journal of Zoology, 45:3, 361-369

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ISRAEL JOURNAL OF ZOOLOGY, Vol. 45, 1999, pp. 361-369

INHERITANCE OF THREE DORSAL COLOR/PATTERN MORPHS IN SOME TURKISH PHILAENUS SPUMARIUS (HOMOPTERA: CERCOPIDAE)

POPULATIONS

SELCUK YURTSEVER

School of Pure & Applied Biology, College of Cardiff, University of Wales, Cardiff CF 1 3TL, UK

ABSTRACT

Laboratory breeding experiments investigated the inheritance of dorsal color/ pattern variation in the meadow spittlebug Philaenus spumarius using mate­rial from two populations from northwestern Turkey. The genetic basis of the polymorphism in the Turkish populations differs from that established for urban Welsh (Great Britain) populations. A preliminary study of the Turkish populations revealed that the trilineatus phenotype is dominant over the marginellus and typicus/populi phenotypes in both sexes. Marginellus is dominant over typicus/populi in females but recessive in males. This model of inheritance differs from urban Welsh populations, where marginellus is domi­nant over typicuslpopuli in both sexes.

INTRODUCTION

The phenomenon of polymorphism has been one of the most discussed subjects in evolutionary biology since Ford (1937) first defined it. Polymorphism of color and pattern in invertebrates has significant effects on fitness (Grant, 1963; Kettlewell, 1973). Numerous examples of transient and stable color/pattern polymorphisms have been found in a wide variety of taxa, including snails (Clarke et al., 1968), butterflies (Sheppard et al., 1985), moths (Kettlewell, 1973), beetles (Kennedy, 1961), and spiders (Oxford, 1983). Genetic control of polymorphism is usually governed by simple or complex allelic systems (Kettlewell, 1973; Lees, 1981; Oxford, 1983). Furthermore, the importance of non-allelic modifiers of the main color locus is well understood (Fisher, 1935; Ford, 1955; Sheppard et al., 1985).

Separated populations may develop genetic divergence over time due to deterministic and stochastic influences (Hedrick, 1985). The factors maintaining polymorphic varia­tion may differ in importance in populations occupying different environments. Certain modes of selection and gene flow may influence genetic diversity (Endler, 1986). Distance between populations or physical barriers to movement may determine the level of gene flow and allow stochastic events to result in differentiation of local populations

tPresent address: Department of Biology, Faculty of the Arts and Science, Thrace University, 22030 Edime,

Turkey. E-mail: selcuky@trakya.edu.tr

Accepted February 1999.

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(Brakefield, 1990; Al-Hiyaly et al., 1993). Since separate populations may experience different ecological factors and selection regimes, the genetic architecture of a polymor­phism cannot be expected to remain constant throughout a species' range.

The highly polyphagous meadow spittlebug Philaenus spumarius is one of the three European species in the genus whose nymphs produce spittle (Drosopoulos and Loukas, 1993). It is one of the most abundant and well-known homopteran species, occurring in most terrestrial habitats throughout the Holoarctic region (Halkka and Halkka, 1990; Stewart and Lees, 1996). Adults show a striking, genetically controlled, color/pattern polymorphism on the dorsal surface (Halkka and Halkka, 1990; Stewart and Lees, 1996). Variations in pigmentation on the ventral surface (Beregovoi, 1970; Svala and Halkka, 1974) are associated with dorsal phenotype (West, 1990; Yurtsever, 1997). The meadow spittlebug is polyandrous (Yurtsever, 1997) and females may mate several times with different males. The resulting multiple paternity probably affects this species' extensive global distribution through increased genetic heterogeneity, as reported in numerous insect species (Smith, 1984).

Stewart and Lees ( 1996) described thirteen dorsal color morphs in adult P. spumarius (denoted by three-letter abbreviations for convenience) (Halkka et al., 1973). Of the 13 morphs, 5 are categorized as non-melanics and are light straw-colored, with dark mottling, or stripes. The remaining morphs are melanics, predominantly black or dark brown with different combinations of pale markings on the dorsal surface. Seven alleles at a single autosomal locus control the expression of the eleven most common pheno­types (Halkka et al., 1973). Two alleles 't' and 'T' represent non-melanic phenotypes, POP (populi) + TYP (typicus) and TRI (trilineatus), respectively. The uniform straw­colored POP is a variety of TYP. The nomenclature TYP/POP indicates either of these two. MAR (marginellus) is one ofthe eight melanics and is expressed by the 'M' allele (Fig. 1).

TYP TRI MAR Fig. 1. Three dorsaUcolor phenotypes of Philaenus spumarius. From left to right: TYP (typicus), TRI (trilineatus), and MAR (marginellus).

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Vol. 45, 1999 INHERITANCE OF DORSAL COLOR/PATTERN IN PHILAENUS SPUMARIUS 363

The dominance hierarchies of 11 commonly occurring phenotypes have been de­scribed for Fennoscandian (Halkka et al., 1973) and urban British populations (Stewart and Lees, 1988). In the latter, TRI is the top dominant phenotype, followed by melanics, and TYP/POP is the bottom recessive in both sexes. However, Fennnoscandian popula­tions feature different dominance relationships in the two sexes: in males, TYP/POP is the second dominant after TRI, and the melanics are the bottom recessives, but in females the dominance hierarchy reflects that of the British model. Some phenotypes are thought to be produced by modifier alleles at secondary loci (Stewart and Lees, 1996). According to Lees (1993), only two different phenotypes-FLA (flavicollis) and TYP/ POP-occur in New Zealand populations of P. spumarius, and FLA is dominant over TYP/POP in both sexes (Yurtsever and Lees, 1994). Inheritance of the 11 main pheno­types in some rural Welsh populations (Yurtsever, 1997) largely follows the model established by Stewart and Lees (1988) for the urban British populations.

The occurrence and frequencies of the dorsal color/pattern morphs vary from location to location (Halkka and Halkka, 1990; Stewart and Lees, 1996). Extensive studies have shown that several deterministic (Stewart and Lees, 1988; Thompson, 1988) and sto­chastic (Brakefield, 1990; Lees, 1993) events, associated with environmental factors (Boucelham et al., 1988) may affect patterns of variation in natural populations of P. spumarius. Melanic phenotypes, particularly MAR, are strictly limited to females in many natural populations (Beregovoi, 1970; Thompson and Halkka, 1973; Boucelham et al., 1988; Brakefield, 1990). However, this limitation does not occur in British populations (Stewart and Lees, 1988). The reasons for the absence of melanics and reversal difference between the sexes in certain populations are still being debated (Halkka et al., 1973; Stewart and Lees, 1987, 1988).

Although the meadow spittlebug is found in Turkey (Lodos, 1986; Zeybekoglu and Kartal, 1988), information on the genetics of its polymorphism is very limited. This is the first report on inherited polymorphism in P. spumarius in Turkey.

MATERIALS AND METHODS

The two sampling sites, Vize and Sogucak, are located in northwestern Turkey, at about 75 m altitude. The area is mainly agricultural and adjacent to forest characterized by Quercus spp. and Rhododendron ponticum. Host plant species recorded for P. spu­marius from these sites were: Cirsium spp., Equisetum arvense, Ornithogalum ortophyllum, Ruscus aculeatus, Silene spp., Trifolium spp., Triticum spp., and Vicia spp.

Meadow spittlebugs were collected as nymphs in early May and used as a broad stock for further experiments. The insects were reared on dwarf broad beans (Viciafaba cv. 'The Sutton') in cylindrical transparent breeding cages (12 x 38 em) made of 0.16 mm 'Agralon' sheeting and fme gauze.

Two rooms with different temperature and photoperiod regimes (West and Lees, 1988) were used for breeding experiments. The nymphs were sexed and females and males were placed in separate cages in the last nymphal instar. Crosses were set up with virgin adult pairs in breeding cages. Most pairs copulated readily, and gravid females

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laid up to 380 eggs. The egg clusters were collected from the cages and were placed in Petri dishes with plaster of Paris base containing 'Nipagin' as antibiotic to protect the eggs from fungal infections and keep them moist. These eggs were refrigerated at< 5 ac for approximately 90 days, and then placed in breeding cages. The majority hatched synchronously within approximately 25 days and were examined under a stereo micro­scope at xlO magnification. Under the laboratory conditions described above, the life cycle was reduced to approximately 6 months, as opposed to a mean average life cycle of about 9 months.

Phenotype frequencies in the progeny were tested for agreement with expected Mendelian ratios using X2 Goodness of Fit test with appropriate degrees of freedom (df). In the crossing experiments, each individual family was given a code number; the letter T (for Turkey) followed by a number identifying the cross. The last two digits represent the year of the experiment. The locality of parental origin (female, then male) is also indicated in parentheses.

RESULTS

Of the 43 crosses set up, only 19 were successful, providing a total of522 progeny. Only four different phenotypes of P. spumarius were obtained from northwestern Turkey. Although crosses were set up with TRI, MAR, FLA, and TYP/POP, only TRI, MAR, and TYP/POP crosses produced offspring. All of these confirmed the dominance of TRI over MAR and TYP/POP in both sexes. In addition, MAR was found to be dominant over TYP/POP in females but recessive in males.

CROSSES INVOLVING PARENTS TRI, MAR, AND TYP/POP

Three TRI x TRI (Table 1) crosses produced 3 TRI and 1 TYP/POP progeny. Although the number of progeny is very small, these results suggest the dominance of TRI to TYP/POP, since TYP/POP offspring occurs in T/35/94. Therefore the TRI parents must both have been heterozygous for TYP/POP (Tit x Tit).

The progeny of T/8/93 (TRI x POP) segregate both of the parental phenotypes. If the female TRI was Tit heterozygous, the data from this family fit a 1: 1 {TRI : TYP/POP) segregation in females (df = 1, r = 0.07, p > 0.05) and in total (df = 1, r = 3.12, p > 0.05). Nevertheless, the data depart from a 1:1 segregation in males (df =I, x2 = 4.26, 0.05 > p > 0.01), due to the excess ofTYP/POP males.

Table 1 shows that T/43/95 (TYP x TRI) produces TRI and MAR phenotypes in females, while producing TRI and TYP/POP phenotypes but no MAR in males. These results indicate that TYP/POP is dominant over MAR in males but recessive in females (see Discussion). In family T/43/95, the female TYP parent originated from T/35/94 (TRI x TRI), and the male TRI parent originated from T/36/94 (MARx TRI). Thus, the male TRI must have been heterozygous for MAR (TIM) since MAR occurs among the female progeny. This family is large enough to test statistically and the data fit to a 1: 1 (MAR: TRI) segregation in females (df = 1,r = 0.47,p > 0.05). The data also agree with 1: I (TRI : TYP/POP) segregation in males (df = I, r = 0.03, p > 0.05). Furthermore, if

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Table 1 Crosses involving parents TRI (trilinetus), MAR (marginellus), and TYP/POP (typicus+populi)

Cross no. Parents Parental provenance Progeny

Female Male Female Male Female Male Total

T/5/93 TRI TRI Sogucak Sogucak 1 TRI

T/24/94 TRI TRI T/8/93 T/8/93 1 TRI (TRI x POP) (TRI xPOP)

T/35/94 TRI TRI T/8/93 T/8/93 1 TRI 2 (TRI xPOP) (TRI xPOP) 1 TYP

T/8/93 TRI POP Sogucak Sogucak 6TRI 5TRI 32 7TYP 12POP

2TYP

T/43/95 TYP TRI T/35/94 T/36/94 19 TRI 16TRI 65 (TRI xTRI) (MARxTRI) 15MAR 15POP

T/36/94 MAR TRI T/2/93 T/8/93 2TRI 5TRI 9 (MARx POP) (TRixPOP) 2MAR

T/2/93 MAR POP Sogucak Sogucak 21 MAR 5POP 61 7TYP 28TYP

T/42/95 MAR POP T/36/94 T/31/93 3MAR 6POP 13 (MARxTRI) (TYPxTYP) 4TYP

the total TRI progeny are examined against the combined MAR and TYP/POP progeny (MAR+TYP/POP), these data fit a l:l segregation (df = I, x!- = 0.38, p > 0.05). Consequently, these results show the dominance of TRI over MAR and TYP/POP in both sexes.

T/2/93 and T/42/95 (Table l) are between MAR females and POP males. Their progeny segregated between MAR and TYP/POP in females but only TYP/POP in males. Therefore, the female MAR parents must have been heterozygous for TYP/POP (Mit) while the male POP parents must have been the tit homozygotes. These results again suggest that MAR is dominant over TYP/POP in females but recessive in males. A total of74 progeny were tested against a 1:1 (MAR: TYP/POP) and departed from the expectation (df = 1, x2 = 4.82, 0.05 > p > 0.01) due to an exce~ of MAR phenotypes among the female progeny.

CROSSES INVOLVING PARENTS BOTH TYPIPOP

A total of 11 successful crosses involved families in which the female and male parents were both TYP/POP (Table 2). Some of the original parents of these families were collected from the wild, while others were F

1 crosses. The resulting progeny were

171 females and 174 males, all of them TYP/POP. As a result, the dominance hierarchy for the three dorsal phenotypes of P. spumarius

from Turkey can be summarized as: "TRI >MAR> TYPIPOP" in females, and "TRI > TYPIPOP >MAR" in males.

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Table 2 Crosses involving parents both TYP/POP (typicus/populi)

Cross no. Parents Parental provenance Progeny

Female Male Female Male Female Male Total

T/1193 TYP POP Sogucak Sogucak 2TYP 4TYP 6

T/6/93 TYP POP Sogucak Sogucak 18TYP 7POP 37 12TYP

Tn/93 TYP POP Sogucak Sogucak 23TYP 18POP 41

T/9/93 TYP POP Sogucak Sogucak 5TYP 2POP 7

T/10/93 TYP TYP Sogucak Vize 45TYP 40TYP 85

T/11/93 TYP TYP Sogucak Vize 21TYP 17TYP 38

T/13/93 TYP POP Sogucak Vize 6TYP 9POP 15

T/16/93 TYP TYP Vize Sogucak 1 TYP

T/21193 TYP TYP Sogucak Sogucak 50TYP 55TYP 105 T/26/94 TYP POP T/8/93 T/13/93 1 TYP

(TRixPOP) (TYP x POP) T/31194 TYP TYP T/1/93 T/1193 2POP 2

(TYPxPOP) (TYPxPOP)

DISCUSSION

Preliminary results from the present breeding experiments with Turkish P. spumarius demonstrate that inheritance of the dorsal color/pattern of the MAR and TYP/POP phenotypes is different from the British model (Stewart and Lees, 1988). MAR is dominant over TYP/POP in both sexes in the British populations, while in Turkish crosses MAR was dominant over TYP/POP only in females, but recessive in males. However, the reversal dominance relationship between MAR and TYP/POP in Turkish P. spumarius is also found in the Finnish populations (Halkka et al., 1973) and several rural Welsh populations (Yurtsever, 1997).

On the other hand, it is not known whether MAR is expressed in male P. spumarius from the Turkish populations as found for the British populations (Stewart and Lees, 1988) or is not expressed as found for many natural populations (Beregovoi, 1970; Thompson and Halkk:a, 1973; Boucelham et al., 1988; Brakefield, 1990). In this respect, penetration of the "M' allele in males from the Turkish populations is questionable. This allele may have variable expressivity (Mettler et al., 1988) due to sex-related genetic influences as reported in the polymorphic spider Enoplognatha ovata (Oxford, 1983). Reversal difference between the sexes for this polymorphism reflects the effects of modifier genes on the major color/pattern locus, causing expression to be inhibited or masked (Stewart and Lees, 1988). Because modifier genes may attain reversal of dominance (Mettler et al., 1988), they may play a significant role in genetic differentia­tion between isolated populations for certain genetic traits (Clarke et al., 1985).

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The crosses demonstrate dominance of TRI over MAR and TYP/POP in the two sexes. Nevertheless, a small number of TRI progeny was produced from TRI x TRI crosses. This implies that some TIT homozygotes may be lethal (similar to some homozygous melanic phenotypes in Halkka and Halkka's (1990) study). On the other hand, it is clear from the progeny that the data do not always follow Mendelian ratios. In fact, total progeny from MAR x TYP crosses are close to a 2:1 ratio when a 1:1 ratio is expected. These results suggest a dominance breakdown, possibly due to modifier alleles at a separate locus (or loci).

The presence of genes at other loci influencing dominance at the observed locus was demonstrated in early studies with Coleoptera (Breitenbecher, 1921), poultry (Fisher, 1935), Lepidoptera (Ford, 1955), and mice (Bodmer, 1960). Ford (1955), working with polymorphic moths, suggested that these genes might vary geographically. Many workers studying color/pattern variation in other species have reported similar findings (Clarke and Sheppard, 1971; Jones et al., 1977; Gillespie and Tabashnik, 1989). All these studies showed examples of dominance breakdown. Stewart and Lees (1987) suggest that the different modes of inheritance in the British and Finnish populations of P. spumarius are probably due to changes at modifying loci, and that the genetic architecture of this polymorphism in the two regions has therefore evolved differently. Similar genetic differences between separated natural populations have also been reported in the African mimetic butterfly (Papilio dardanus) which is polymorphic for wing color/patterns (Clarke et al., 1985). Thus, observed genetic clifferences between populations of a polymorphic species may not only be due to primary genes, but the influence of modifiers must also be borne in mind (Gordon and Gordon, 1957). Fisher (1928) already proposed that dominance is a modifiable parameter, which evolved as the result of selection for modifiers (Clarke and Sheppard, 1960). The present study shows another example in which the genetic architecture of natural populations could have been changed by modifiers. These results also shed light on the absence of MAR males in many natural populations (Beregovoi, 1970; Thompson and Halkka, 1973; Boucelham et al., 1988; Brakefield, 1990). In isolated populations dominance modi­fication may develop to opposite directions, resulting in a certain trait becoming dominant in one population but recessive in another (Stewart and Lees, 1988). Modifier genes for the MAR phenotype as well as other phenotypes may have evolved differently in isolated natural populations of P. spumarius due to selection of modifiers.

Genetic differences concerning the MAR and TYP/POP phenotypes between previ­ously studied P. spumarius populations (Halkka et al., 1973; Stewart and Lees, 1988) and the Turkish populations presented here are not surprising, since there is significant geographic isolation between these populations, along with differences in ecological factors. Widely separated populations under variable environmental conditions will show different genetic response to evolutionary forces (Ward and Warwick, 1980). In the future, extended surveys concerning other phenotypes of P. spumarius, as well as other populations occurring in Turkey, may reveal additional subtle differences from previously investigated populations.

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ACKNOWLEDGMENTS

I would like to thank Prof. John Fry for use of the college facilities, and Dr. David Lees for his guidance and help during the research at the University of Wales, Cardiff College. I am very grateful to the Turkish Government for providing the research grant.

REFERENCES

Al-Hiyaly, S.A.K., McNeilly, T., Bradshaw, A.D., and Mortimer, A.M. 1993. The effect of zinc contamination from electricity pylons. Genetic constraints on selection for zinc tolerance. Heredity 70: 22-32.

Beregovoi, V.E. 1970. Differences in colour variation in males and females of the common froghopper Philaenus spumarius (L.). Dokl. Akad. Nauk SSSR 191: 1156-1159 (in Russian).

Bodmer, W.F. 1960. Interaction of modifiers: The effect of pallid and fidget on polydactyly in the mouse. Heredity 14: 445-448.

Boucelham, M., Hokkanen, H., and Raatikainen, M. 1988. Polymorphism of Philaenus spumarius (L.) (Homoptera, Cercopidae) in different latitudes, altitudes and habitats in the U.S.A. Ann. Entomol. Fenn. 54: 49-54.

Brakefield, P.M. 1990. Genetic drift and patterns of diversity among colour-polymorphic popula­tions of the homopteran Philaenus spumarius in an island archipelago. Bioi. J. Linn. Soc. 39: 219-237.

Breitenbecher, J.K. 1921. The genetic evidence of a multiple (triple) allelomorph system in Bruchus and its relation to sex-limited inheritance. Genetics 6: 65-90.

Clarke, B., Diver, C., and Murray, J. 1968. Studies on Cepaea. VI. The spatial and temporal distribution of phenotypes in a colony of Cepaea nemoralis (L.). Philos. Trans. R. Soc. Lond. B 253: 519-548.

Clarke, C.A. and Sheppard, P.M. 1960. The evolution of dominance under disruptive selection. Heredity 14: 73-86.

Clarke, C.A. and Sheppard, P.M. 1971. Further studies on the genetics of the mimetic butterfly Papilio memnon L. Philos. Trans. R. Soc. Lond. B 263: 35-70.

Clarke, C., Clarke, F.M.M., Collins, S.C., Gill, A.C.L., and Turner, J.R.G. 1985. Male-like females, mimicry and transvestism in butterflies (Lepidoptera: Papilionidae). Syst. Entomol. 10: 257-283.

Drosopoulos, S. and Loukas, M. 1993. Population studies ofthe spittlebug genus Philaenus in the Mediterranean. Proc. 8th Auchenorrhyncha Congr. Delphi, Greece, pp. 98-99.

Endler, J.A., ed. 1986. Natural selection in the wild. Princeton University Press, Princeton, NJ. Fisher, R.A. 1928. Two further notes on the origin of dominance. Am. Nat. 62: 571-574. Fisher, R.A. 1935. Dominance in poultry. Philos. Trans. R. Soc. Lond. B 225: 197-226. Ford, E.B. 1937. Problems of heredity in the Lepidoptera. Bioi. Rev. 12: 461-503. Ford, E.B. 1955. Polymorphism and taxonomy. Heredity 9: 255-264. Gillespie, R.G. and Tabashnik, B.E. 1989. What makes a happy face: Determinants of colour

pattern in the Hawaiian happy-face spider Theridion grallator (Araneae, Theridiidae). Hered­ity 62: 355-363.

Gordon, H. and Gordon, M. 1957. Maintenance of polymorphism by potentially injurious genes in eight natural populations of the platyfish, Xiphophorus maculatus. Genetics 55: 1-44.

Grant, V. 1963. The origin of adaptations. Columbia Univ. Press, New York. Halkka, 0. and Halkka, L. 1990. Population genetics of the polymorphic meadow spittlebug,

Philaenus spumarius (L.). Evol. Bioi. 24: 149-191.

Dow

nloa

ded

by [

Nov

a So

uthe

aste

rn U

nive

rsity

] at

03:

31 0

8 O

ctob

er 2

014

Vol. 45, 1999 INHERITANCE OF DORSAL COLOR/PATTERN IN PHILAENUS SPUMARIUS 369

Halkka, 0., Halkka, L., Raatikainen, M., and Hovinen, R. 1973. The genetic basis of balanced polymorphism in Philaenus (Homoptera). Hereditas 74: 69-80.

Hedrick, P.W. 1985. Genetics of populations. Jones and Bartlett, Boston. Jones, J.S., Leith, B.H., and Rawlings, P. 1977. Polymorphism in Cepaea: A problem with too

many solutions. Annu. Rev. Ecol. Syst. 8: 109-143. Kennedy, J.S. 1961. Insect polymorphism. Symp. R. Entomol. Soc. Lond. 1: 1-115. Kettlewell, B. 1973. The evolution of melanism. Clarendon Press, Oxford. Lees, D.R. 1981. Industrial melanism: Genetic adaptation to air pollution. In: Bishop, J.A. and Cook,

L.M., eds. Genetic consequences of man made change. Academic Press, London, pp. 129-176. Lees, D.R. 1993. Novel New Zealand populations of the meadow spittlebug Philaenus spumarius

(Cercopidae). Proc. 8th Auchenorrhyncha Congr. Delphi, Greece, pp. 95-97. Lodos, N. 1986. Entomology. Ege University Press, Izmir, Turkey. Mettler, L.E:, Gregg, T.G., and Schaffer, H.E. 1988. Population genetics and evolution. Prentice­

Hall, Englewood Cliffs, NJ. Oxford, G.S. 1983. Genetics of colour and its regulation during development in the spider

Enoplognatha ovata (Clerk) (Aranea: Theridiidae). Heredity 51: 621-634. Sheppard, P.M., Turner, J.R.G., Brown, K.S., Benson, W.W., and Singer, M.C. 1985. Genetics

and evolution of Muellerian mimicry in Heliconius butterflies. Philos. Trans. R. Soc. Lond. B 308: 433-610.

Smith, R.L. 1984. Sperm competition and the evolution of animal mating systems. Academic Press, London.

Stewart, A.J.A. and Lees, D.R. 1987. Genetic control of colour polymorphism in spittlebugs (Philaenus spumarius) differs between isolated populations. Heredity 59: 445-448.

Stewart, A.J.A. and Lees, D.R. 1988. Genetic control of colour/pattern polymorphism in British populations of the spittlebug Philaenus spumarius (L.) (Homoptera: Aphrophoridae). Bioi. J. Linn. Soc. 34: 57-79.

Stewart, A.J.A. and Lees, D.R. 1996. The colour/pattern polymorphism of Philaenus spumarius (L.) (Homoptera: Cercopidae) in England and Wales. Philos. Trans. R. Soc. Lond. B 351: 69-89.

Svala, E. and Halkka, 0. 1974. Geographic variability of frontoclypeal polymorphism in Philaenus spumarius (L.) (Homoptera). Ann. Zoo!. Fenn. 11: 283-287.

Thompson, V. 1988. Parallel colour form distributions in European and North American popula­tions of the spittlebug Philaenus spumarius (L.). J. Biogeogr. 15: 507-512.

Thompson, V. and Halkka, 0. 1973. Color polymorphism in some North American Philaenus spumarius (Homoptera:Aphrophoridae) populations. Am. Midi. Nat. 89: 348-359.

Ward, R.D. and Warwick, T. 1980. Genetic differentiation in the molluscan species Littorina rudis and Littorina arcana (Prosobranchia: Littorinidae). Bioi. J. Linn. Soc. 14: 417-428.

West, J. 1990. Aspects of ventral colour/pattern variation in the spittlebug Philaenus spumarius. M.Phil. thesis, University of Wales, Cardiff.

West, J. and Lees, D.R. 1988. Temperature and egg development in the spittlebug Philaenus spumarius (L.) (Homoptera:Aphrophoridae). Entomologist 107: 46-51.

Yurtsever, S. 1997. Inheritance of colour/pattern variation in the meadow spittlebug Philaenus spumarius. Ph.D. thesis, University of Wales, Cardiff.

Yurtsever, S. and Lees, D.R. 1994. Inheritance of the dorsal colour/pattern polymorphism of the meadow spittlebug, Philaenus spumarius (L.) (Homoptera) (Cercopidae) in New Zealand populations. Proc. 12th Nat. Biology Congr., Edirne, Turkey, pp. 195-201.

Zeybekoglu, U. and Kartal, V. 1988. Morph variations of Philaenus spumarius (Homoptera, Auchenorrhyncha, Cercopidae) in Samsun province. Proc. 9th Nat. Biology Congr., Samsun, Turkey, pp. 171-175.

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