Biologia 65/2: 309—315, 2010 Section Zoology DOI: 10.2478/s11756-010-0022-x

The colour/pattern polymorphism of spumarius (: ) in the north-western Black Sea region of Turkey

Selcuk Yurtsever, Nilgun Akdeniz &BurcuKarahalil

Biology Department, Faculty of the Arts and Science, Trakya University, 22030 Edirne, Turkey; e-mail: [email protected]

Abstract: The heritable elytral colour/pattern polymorphism of in north-western Black Sea region of Turkey was investigated. A total of 2,530 adult spittlebugs, 1,020 females and 1,510 males were collected and analysed in terms of the 11 most common colour forms. Nine different phenotypes, expressed by six different alleles, were determined: populi (POP), typicus (TYP), trilineatus (TRI), marginellus (MAR), flavicollis (FLA), leucocephalus (LCE), gibbus (GIB), albomaculatus (ALB), and leucophtalmus (LOP). The common phenotypes lateralis (LAT) and quadrimaculatus (QUA) of previous studies were not encountered at all. The predominant phenotype was TYP (63%) in females and males followed by POP (31%). TRI (4%) and melanics (5%) were at close proportions. However, only one site had nine phenotypes altogether. The majority of the sites had only the POP and TYP morphs. The melanic forms were found only in females. Key words: polymorphism; meadow spittlebug; Philaenus spumarius; Hemiptera; Cercopidae; Turkey

Introduction al. 1988; Halkka et al. 2001; Quartau & Borges 1997). Moreover, melanics are usually expressed in females The adults of the meadow spittlebug Philaenus spuma- only. In New Zealand populations only POP, TYP and rius (L., 1758) are polymorphic for its dorsal colour/pat- FLA have been found to occur (Lees 1993; Hodge & tern. It has been recorded from numerous habitats in Keesing 2000). The pattern of frequency distribution the temperate and humid parts throughout the Holarc- dealing with non-melanics and melanics usually ex- tic region (Weaver & King 1954; Boucelham et al. 1988; hibits close resemblance in many populations. TYP and Halkka & Halkka 1990; Stewart & Lees 1996; Yurt- POP generally predominate over the remaining pheno- sever 2000). Although more than 16 different pheno- types. However, a few local populations sharply devi- types (Yurtsever 2000) have been known to occur in ate from this general pattern. For example, in several its world-wide distribution, 11 of the phenotypes are British populations (Lees & Dent 1983) melanics are most common (Halkka & Halkka 1990; Stewart & Lees expressed in both sexes and non-melanic phenotype fre- 1996). Three of the phenotypes are non-melanics – POP quencies remain just around five percent where melanic (populi), TYP (typicus), and TRI (trilineatus)–and phenotypes show great genetic adaptations to changing are light straw coloured with dark mottling, or stripes environmental conditions on the dorsal surface. The remaining are melanics – Along with environmental conditions (Halkka et MAR (marginellus), LAT (lateralis), FLA (flavicollis), al. 1976; Lees & Dent 1983; Boucelham & Ratikainen GIB (gibbus), LCE (leucocephalus), QUA (quadrimacu- 1984; Quartau & Borges 1997), different evolutionary latus), ALB (albomaculatus), and LOP (leucopthalmus) elements in a variety of populations influence these – predominantly black or dark brown with different variations. Several selective agents (Owen & Wiegert combinations of pale markings (Fig. 1). The polymor- 1962; Halkka & Mikkola 1965; Whittaker 1972; Berry phism is heritable and seven alleles at an autosomal & Willmer 1986; Thompson 1988) are highly correlated locus control the expression of the single or a group of with the level of melanism. On the other hand, some similar phenotypes (Halkka & Halkka 1990; Stewart & small island populations (Brakefield 1990; Lees 1993; Lees 1996). Halkka et al. 2001) provide strong evidence how the Remarkable geographic variation in the occurrence genetic drift events shape these geographic variations. and frequencies of the dorsal phenotypes of P. spumar- There are few studies dealing with the polymor- ius have been demonstrated. Although 11 common phe- phism of P. spumarius in Turkey. The three studies notypes occur in the most natural populations stud- involve the Istranca Mts (Yurtsever & Sal 2003) and ied, some melanics in several populations are rare or some other Trakya populations (Yurtsever 2001) in NW absent (Halkka 1964; Whittaker 1972; Thompson & Turkey. A recent great deal of data include mid Black Halkka 1973; Vilbaste 1980; Honěk 1984; Boucelham et Sea region populations (Zeybekoglu et al. 2004). The

c 2010 Institute of Zoology, Slovak Academy of Sciences 310 S. Yurtsever et al.

and hills (up to 2,500 m a.s.l.) The mountains ranges of- ten separated by deep river valleys. The sampling period covered the months of June and July in the years of 2005, 2006 and 2007. A total of 46 samples were performed in 42 sites where P. spumarius occurred in 19 sites only. All the sites were rural and included different habitat types ranging from forests to meadows. The adult spittlebugs were col- lected from herbaceous plants in humid places nearby water sources, such as meadows, streamsides, lakesides and road- sides. A standard sweeping net and a sucking aspirator were used for the sampling of the . About one hour was spent in each sampling session. Specimens were examined in the laboratory under a binocular stereomicroscope. A total of 2,530 spittlebugs (1,020 females and 1,510 males) were analysed in the three years of study (Table 1). The phenotypes of the meadow spittlebugs were sexed and classified according to Halkka et al. (1973) and Stewart & Lees (1996). The phenotypes were in general clearly ex- pressed in the insects but a few specimens were difficult to score. Five LCE-like, male spittlebugs were unclear and therefore excluded from the analyses. The study involved a total 46 samplings from 42 sites in which only 23 samplings in 19 sites (Fig. 2) had P. spumar- ius. Most of the samples included a few (<20) spittlebugs. Only four of the study sites included a satisfactory num- ber of specimens for the statistical analyses, namely in the Duzce (200 m a.s.l.), Gerede (1330 m a.s.l.), Cerkes (1200 m a.s.l.), and Azdavay (850 m a.s.l.) provinces of Turkey. These sites had different habitat properties. The site in Duzce was a large abandoned field along a streamside. The site in Gerede was a meadow nearby a stream. The Cerkes was an evergreen large meadow nearby a lake. The site in Azdavay was a meadow nearby a stream in the forest. The Chi-Squared Contingency Test (R × C) with an appropriate degree of freedom (df) was used to show whether or not differences occurred in the proportions of the phenotype groups among the sites and along the years regarding four sites that had appropriate data for the sta- tistical analyses.. Frequencies of the two sexes and the data in were combined to obtain appropriate data for the tests in the four study sites mentioned above.

Results

In the majority of the samples, the numbers of the meadow spittlebug were very scarce even though the vegetation was apparently good enough for the survival Fig. 1. The most common dorsal colour/pattern phenotypes of of the insects. The number of the specimens varied in Philaenus spumarius. (The abbreviations are given in the text). the samples. The average number of the spittlebugs was From left to right, in top row: TRI and TYP. The second row: 133 for 19 sampling. As a result, nine different dorsal MAR and LAT. The third row: FLA, GIB, LCE. The bottom colour/pattern phenotypes (POP+TYP, TRI, MAR, row: QUA, ALB, LOP (The uniformly light coloured POP is not given for convenience). FLA, GIB+LCE, and ALB+LOP) expressing six dif- ferent alleles (“t, T, M, F, C, and O” respectively) oc- curred in the north-western Black Sea region of Turkey. present study was carried out to determine the poly- The lateralis (LAT) phenotype (expressed by the allele morph frequency in the north-western Black Sea region “L”), which is one of the common forms in most Phi- of Turkey. laenus spumarius populations in previous studies was not found. On the other hand, FLA, ALB and LOP phenotypes were found only in Azdavay and GIB and Material and methods LCE phenotypes occurred only in Duzce and Azdavay. This study was carried out throughout the north-western Moreover, melanic phenotypes were limited to females, Black Sea region of Turkey (Fig. 2). This region contains and, although it was unclear, 5 males resembling the productive forests (Kaya & Raynal 2001) on the mountains morph GIB were most likely dark POP forms. Polymorphism in northern Turkish Philaenus spumarius 311

Fig. 2. The schematic map of the north-western Black Sea region of Turkey showing four sites where appropriate data used in the analyses and the other 15 sites where Philaenus spumarius (dots) occurred in the samples. The squares show main cities in the area.

(66) (101) (55) (35) (55) 4% 4% 3% 2% 5% (149) 15% (779) 31% (630) (809) 42% 54% (1590) 63% (781) 77%

TRI Combined melanics POP TYP

Fig. 3. Percentages of the dorsal colour/pattern phenotypes of Philaenus spumarius found in the north-western Black Sea region of Turkey (sample size in parenthesis). Circles from left to right indicate combined sexes, males, and females, respectively.

Table 1. Frequencies of the seven different colour/pattern phenotype groups in Philaenus spumarius collected from the NW Black Sea region of Turkey during the three years study.

POP TYP TRI MAR FLA ‘C’ group ‘O’ group Total

 ¾  ¾  ¾ ¾ ¾ ¾ Year / Site ¾

2005 / Duzce 4 8 24 11 3 1 1 0 1 0 53 2005 / Gerede 5 30 33 30 1 0 3 0 0 0 102 2005 / Other sites 2 1 2 3 0 0 0 0 1 0 9 2006 / Azdavay 12 49 65 44 7 10 2 2 2 0 193 2006 / Cerkes 21 67 94 62 0 0 3 0 0 0 247 2006 / Other sites 2 5 6 4 1 0 0 0 0 0 18 2007 / Duzce 9 12 18 17 2 6 1 0 2 0 67 2007 / Gerede 0 6 10 16 0 0 0 0 0 0 32 2007 / Azdavay 38 190 191 240 21 47 7 3 4 4 745 2007 / Cerkes 49 246 275 318 0 2 18 0 0 0 908 2007 / Other sites 7 16 63 64 0 0 1 0 0 0 151

As can be seen in Fig. 3, the predominant pheno- (4%) is higher than melanics (2%) in overall data, but type is TYP in overall, in males and in females (63%, melanics (5%) are higher than TRI (3%) in females. 54%, 77%, respectively) followed by POP (31%, 42%, There is no melanics in males. 15%, respectively). The proportions of TRI and com- Due to the very low number of the specimens in bined melanics are very close, these two categories are the samples, the frequency differences of the phenotypes much less than POP and TYP. The proportion of TRI were only possible to be statistically compared in the 312 S. Yurtsever et al.

Table 2. The chi-squared test results dealing with the frequency covered with forests which have mixtures of conifer- distributions of Philaenus spumarius between the years in the ous trees dominated by Pinus sylvestris L., P. brutia four sites of the NW Black Sea populations. Ten., P. nigra Arnold. subsp. pallasiana, Picea orien- Population X2 df P talis (L.), Abies spp. (Kaya & Raynal 2001) and agricul- tural fields with wheat are scarce. On the other hand, Duzce 1.681 1 0.195 these scarce agricultural fields get very dry in summer. Gerede 3.215 1 0.073 As a result, the meadow spittlebug seems very sensi- Cerkes 0.692 1 0.406 Azdavay 0.111 2 0.946 tive to extreme climatic conditions even if it has been reported from throughout the Holarctic region (Weaver & King 1954; Boucelham et al. 1988; Halka & Halkka 1990; Yurtsever 2000). The general distribution pattern of the pheno- four sites mentioned above. In the pooled data, again types in the area is similar to previous studies (Halkka only distributions of TYP and POP were possible to 1964; Whittaker 1972; Boucelham & Raatikainen 1984; compare in the four sites which revealed no significant Boucelham et al. 1988). In fact, TYP is the predomi- difference (X2 = 0.815, df = 3, P = 0.846). The pooled nant form followed by POP and TRI and melanics con- data were large enough to compare the frequencies of tribute with small proportions to the pooled data and, the three categories of POP, TYP and melanics among finally, TYP is predominant in both sexes. The propor- Duzce, Cerkes and Azdavay. The test showed no signif- tion of TRI is also parallel to the studies performed icant difference (X2 = 5.053, df = 4, P = 0.283) among in Spain (Quartau & Borges 1997) Ukraine (Halkka et these three sites. Hence, these results seem to indicate al. 1980), Scandinavia (Halkka & Halkka 1990), and that there is no association between certain phenotypes the USA (Boucelham et al. 1988) where it has been and habitat types. usually reported less than 5%. The higher frequencies The frequency distributions of the POP and TYP of TRI in isolated small island populations (Berry & phenotypes regarding the appropriate data between the Willmer 1986; Brakefield 1990) are generally attributed years of 2005 and 2007 for the Duzce and Gerede sites, to stochastic events. The present results differ from and between the years of 2006 and 2007 for Cerkes, as those which previously surveyed three other popula- well as of the POP, TYP, TRI and melanics between tions of Turkey (Yurtsever 2001; Yurtsever & Sal 2003; the years of 2006 and 2007 in Azdavay were compared. Zeybekoglu et al. 2004). In all those three populations, However, the chi-squared tests revealed that the relative the predominant phenotypes proved to be TYP in fe- frequencies of the phenotype categories did not change males and POP in males. Although nine different phe- between the years studied (Table 2). notypes were found in the present study, only one lo- Other spittlebugs were encountered in several sam- cality had the whole number of phenotypes. Most of ples, namely, vulnerata (Rossi, 1807), C. san- the sites usually included TYP and POP only. In the guinolenta (Scopoli, 1763), lineatus (L., New Zealand populations (Lees 1993; Hodge & Keesing 1758), N. campestris (Fallen, 1805), N. exclamations 2000) only three phenotypes with two alleles have been (L., 1784), alni (L., 1805), and Lepyronia knowntooccur.InafewpopulationsinRussia(Whit- coleoptrata (L., 1758). taker 1972; Vilbaste 1980), many phenotypes appear to be lacking since only TYP and POP have been found. Discussion Moreover, LAT, which is one of the common melanic phenotypes in the meadow spittlebug’s world-wide dis- In the present study, the meadow spittlebug P. spuma- tribution (Boucelham & Raatikainen 1987; Halkka & rius was not widely found in the majority of the sites of Halkka 1990; Stewart & Lees 1996), was not found in the north-western Black Sea population. In fact, most the NW Black Sea population here investigated. This samples did not include any specimens at all and only may be an effect of the size of the populations, which two sites had a high number of specimens. Therefore, it might be too small, and the lack of the polymorphism appears that this species is not able to settle well in this give the impression of genetic drift (Brakefield 1990; area. This may be due to the mountainous geographic Lees 1993). On the other hand, the presence of the high pattern of the area which has highly cold and long win- mountains in the area may have affected the gene flow ters and therefore do not offer adequate conditions for among the populations. Thus, it seems that determinis- the survival of the nymphs. These results parallel the tic influences (Halkka & Halkka 1990) override stochas- suggestions of Halkka & Halkka (1990) that high ele- tic events (Berry & Willmer 1986; Brakefield 1990) in vations and cold climate limit the distribution of the Turkish P. spumarius populations. species. Thus, some humidity and mild climatic condi- The situation of the “L” allele and the “O” group tions are the most important factors affecting survival alleles have particular attention in Turkish populations. of the delicate meadow spittlebugs at all stages as sug- Halkka et al. (1973) suggested that LOP and TYP gested by Weaver & King (1954). Agricultural practices are the oldest forms in the evolution of P. spumarius also matter (Lees 1993), such as the presence of hay is pigmentation polymorphism, because these two pheno- an important material for transporting the eggs of the types are genetically recessive two the other all other P. spumarius from place to place. The area is mostly phenotypes in the dominance hierarchy. They men- Polymorphism in northern Turkish Philaenus spumarius 313 tioned that the further mutations have gradually pro- these studies, the shell colour/pattern variation in these duced the LAT and LCE, then “M” allele of MAR has snails exhibits a complex spatial pattern in which have been established by duplication in an L/C (LAT/LCE) interesting steep morph clines in different part of its heterozygote. This postulation was based on the hy- range. For example, at certain geographic scale, tran- pothesis of Sheppard (1971) which points out that dom- sition between regions those have particular morphs inance hierarchy in polymorphism develops gradually are often very sharp associating with climatic factors. and is enhanced by disruptive and frequency dependent But some morph frequencies among some populations selection. The occurrence of TYP in every single popu- change substantially over short distances or show no dif- lation studied previously, support the idea of Halkka et ference even they have similar or reverse environmental al. (1973). It may also be true that the colour/pattern conditions. All these studies as in the other polymor- polymorphism in P. spumarius is mostly result of chro- phic species (Sheppard 1971; Berry 1977; Kettlewell mosomal fusions as it has been demonstrated in the 1973; Endler 1977; White 1978; Roughgarden 1996) close taxa (Marya˜nska-Nadachowska 2002; Marya˜nska- have proved that polymorphic variation in different Nadachowska et al. 2008; Kuznetsova et al. 2009). How- populations of Cepaea is shaped with a variety of evolu- ever the situation of the alleles present or absent in tionary forces (Cook 1998) for thousands of years (Cain Turkish P. spumarius populations does not seem to be 1971). The findings of the present study show a close re- consistent with Halkka et al. (1973). Thus, Turkish pop- semblance to Cepaea and the other species which have ulations will bring out a new discussion on the evolu- parallel polymorphism in many aspects. Because, there tion of polymorphism in P. spumarius. Nevertheless, are significant differences between the north-western the progressing molecular genetic works (Seabra et al. Black Sea populations and recently studied P. spumar- in litt.) will probably shed light at least to some extent ius populations of Turkey (Yurtsever 2001; Yurtsever & on this remarkable polymorphism. Sal 2003; Zeybekoglu et al. 2004). There is a tendency In the North-western Black Sea populations, mela- that geographic variation in the Turkish P. spumarius nics were found at very low frequencies and were lim- populations is somewhat clinal. These clines and their ited to females. This is the usual situation, not only for steepness may have been shaped by not only climatic the previously studied three Turkish populations but conditions (Thompson 1984; Berry & Willmer 1986), also for many European (Halkka 1964; Whittaker 1972; the area effects (Halkka & Halkka 1990; Cook 1998) Honek 1984; Quartau & Borges 1997; Halkka et al. along with the dispersal history (Roughgarden 1996) 2001) and North American (Thompson & Halkka 1973; of P. spumarius may have fundamental influences on Boucelham et al. 1988) populations. The melanic limi- the local evolution (Lees & Dent 1983) of particular tation to the females is usually affiliated with particular morphs. This spittlebug has passive flight ability and genetic influences which may show geographic variation cannot move long distances. Moreover, there is a signif- (Halkka et al. 1980; Stewart & Lees 1996; Yurtsever icant distance among the populations studied. Thus, it 1999). However, laboratory genetic studies supporting is assumed that physical barriers restrict the dispersal such genetic interactions are few (Halkka et al. 1973; in the range of P. spumarius resulting in population di- Yurtsever 1999). Therefore, detailed laboratory genetic vergence where particular allele is favoured in certain studies on the polymorphism of P. spumarius are still population and the other allele is favoured elsewhere. needed in the future to better understand the melanic If there is no physical barrier to dispersal influencing limitation to females. the strength of selection, modifier genes which influ- Most of the sites surveyed in the present study were ence the main colour pattern locus of polymorphism found at high elevations with cool climatic conditions. may play role on the modes of adaptation (Jones et According to the thermal selection hypothesis (Ket- al. 1977; Mikkola 1984; Mettler et al. 1988; Wiehe & tlewell 1973) melanic forms of P. spumarius (Thomp- Slatkin 1998). In P. spumarius, the main pigmentation son 1984; Berry & Willmer 1986) are found at higher locus of polymorphism is closely associated with a small frequencies than non-melanics at the cooler places of number of linked genes (Halkka et al. 2001) which shape higher elevations. However, present study gave no ev- the genetic architecture of geographically isolated pop- idence for this hypothesis. In fact, Azdavay had such ulations. climatic conditions and a very low frequency of melan- Our molecular analyses comparing the data ob- ics. However, the evolutionary history of the species in tained from this study and from some other world pop- this area is still unknown. Thus, it can be considered ulations revealed interesting results (Seabra et al. in that certain populations in the area are well isolated litt.). That is, there is a close molecular genetic rela- and perhaps have conserved stable gene pools. tionship between the Turkish (particularly Cerkes site) The shell colour/pattern polymorphism in the land and Finnish populations regarding certain haplotypes snails of the genus Cepaea,particularlyinC. nemoralis in the phylogenetic tree. This suggests that the Finnish has been one of the best examples for population ge- populations have probably originated from the Turkish netic studies. A great number of snails have been anal- population studied here. However presently, the genetic ysed for decades from many European populations resemblance between these populations is questionable, (Carter 1968; Jones et al. 1977; Mazon et al. 1987; perhaps needs more experimental evidence. Ozgo 2005; Cook 2008) and recently from some North In conclusion, the present study showed once more American populations (Whitson 2005). According to that P. spumarius is a good species for studying evo- 314 S. 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