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On the meadow spittlebug Philaenus spumarius

Authors:
  • Trakya University, Turkey.

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Abstract: Due to its interesting biological aspects, the meadow spittlebug Philaenus spumarius has received great attention from biologists for decades. It has been one of the extensively studied species in ecology and genetics. This homopteran insect shows very high habitat diversity and therefore has a wide global distribution. Adults exhibit a heritable colour/pattern polymorphism on the dorsal surface throughout its range. A similar colour/pattern variation also occurs in certain ventral parts. Recent laboratory studies have dealt with its polyandrous aspect that is, females may mate several times with different males and the offspring of a single female may be fathered, therefore, by several males. Although the effects of multiple mating on natural populations of P. spumarius are not well known, it may have great evolutionary importance through increased genetic heterogeneity and high fitness. Key Words: Meadow spittlebug, Philaenus spumarius, Homoptera, Cercopidae, polymorphism, melanism, genetics, polyandry
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Introduction
Spittlebugs and their nymphal protection have
received attention from biologists for centuries.
Interesting theories have been proposed for the origin of
spittlemasses found on plants in spring. The cuckoo bird
has been suggested as a reason, since this summer
migrant appears in Europe at the same time as the first
spittle masses (1). Therefore this theory gives rise to the
name cuckoo-spit insects. In the literature, spittlemasses
have been called GowkÕs spittle, frog spit, toad spit, snake
spit, witchÕs spit and wood sear. It has also been
suggested that some plants are able to produce spittle
masses. It has even been cited that spittle masses
generate small locusts (2).
It is now known that the spittle masses that are seen
on many plants in spring are produced by the nymphs of
the spittlebugs in the family Cercopidae, which surrounds
their delicate soft body and gives them some protection
from predators and desiccation. The spittlebugs are
homopteran bugs in the superfamily Cercopoidea. This
group currently contributes approximately 2380 species
to the Homoptera (3), and all are Òxylem-feedersÓ and
Òphloem-feedersÓ both as nymphs and adults (4). They
occur on almost all types of plants. Since the nymphs live
Turk J Zool
24 (2000) 447-459
@ T†BÜTAK
447
On the Polymorphic Meadow Spittlebug,
Philaenus spumarius
(L.)
(Homoptera: Cercopidae)
Sel•uk YURTSEVER
Trakya University, Faculty of the Arts and Science, Department of Biology, 22030 Edirne - TURKEY
Received: 13.04.1999
Abstract: Due to its interesting biological aspects, the meadow spittlebug
Philaenus spumarius
has received great attention from
biologists for decades. It has been one of the extensively studied species in ecology and genetics. This homopteran insect shows very
high habitat diversity and therefore has a wide global distribution. Adults exhibit a heritable colour/pattern polymorphism on the
dorsal surface throughout its range. A similar colour/pattern variation also occurs in certain ventral parts.
Recent laboratory studies have dealt with its polyandrous aspect that is, females may mate several times with different males and
the offspring of a single female may be fathered, therefore, by several males. Although the effects of multiple mating on natural
populations of
P. spumarius
are not well known, it may have great evolutionary importance through increased genetic heterogeneity
and high fitness.
Key Words: Meadow spittlebug,
Philaenus spumarius
, Homoptera, Cercopidae, polymorphism, melanism, genetics, polyandry
Polimorfik ‚ayÝr KšpŸk BšceÛi,
Philaenus spumarius
L. (Homoptera: Cercopidae)
†zerine Bir Derleme
…zet: ‚ayÝr kšpŸk bšceÛi olarak bilinen
Philaenus spumarius
, ilgin• biyolojik šzelliklerinden dolayÝ uzun yÝllardÝr biyologlarÝn bŸyŸk
ilgisini •ekmißtir. Bundan dolayÝ ekoloji ve genetikte en •ok •alÝßÝlan tŸrlerden birisi olmußtur. Bir homopter olan bu bšcek •ok •eß
itli habitatlarda yaßayabildiÛinden dŸnyada geniß bir daÛÝlÝma sahiptir. Erginleri bŸtŸn daÛÝlÝm alanÝnda, genetik olarak kontrol edilen
dorsal renk ve desen polimorfizmi gšsterir. Benzer bir renk ve desen varyasyonu aynÝ zamanda ventral yŸzeyde de gšrŸlŸr.
YakÝn zamanda yapÝlan laboratuvar •alÝßmalarÝ, bu tŸrŸn poliandri ile ilgili šzelliklerini ortaya koymußtur. Dißi
P. spumarius
bireyleri
yaßam devrelerinin Ÿreme periyodunda birden fazla erkekle defalarca •iftleßebilir. Sonu•ta tek bir dißiden bir defada meydana gelen
yavrularÝn babalarÝ farklÝ olabilir. PoliandriÕnin bu tŸrŸn doÛal populasyonlardaki evrimsel ve diÛer etkileri tam olarak bilinmemekle
beraber, bu davranÝß
P. spumarius
populasyonlarÝnda genetik •eßitliliÛi arttÝrabilir ve dolayÝsÝyla bu tŸrŸn evrimsel baßarÝsÝnda šnemli
bir faktšr olabilir.
Anahtar SšzcŸkler: ‚ayÝr kšpŸk bšceÛi,
Philaenus spumarius
, Homoptera, Cercopidae, polimorfizm, melanizm, genetik, poliandri
in masses of froth, they are commonly called spittlebugs,
but are also known as froghoppers from their adult
leaping ability (5). The nymphs derive their nourishment
from xylem elements by piercing them with their stylets
and sucking the sap. The spittle is derived from fluid
voided from the anus and from a surfactant secreted by
epidermal glands on the seventh and eighth abdominal
segments. Air bubbles are introduced into the spittle by
means of the caudal appendages of the insect (6). A
spittlebug nymph usually rests head downward on the
plant, and as the spittle forms, it flows down over and
covers the nymph, providing the nymph with a moist
habitat. Adults are free living individuals and do not
produce spittle.
There are ten British Cercopid species producing
spittle (1), and three European species are known in the
genus
Philaenus
(7,8).
P. signatus
and
P. loukasi
are two
of these. The third
P. spumarius
is the most abundant,
and is usually known as the meadow spittlebug. There is
a large body of literature about it, dating from late
sixteenth century (2). The studies dealing with
P.
spumarius
can be grouped into two categories. The first
category involves surveys of its noxious effects as a
serious pest on cultivated and wild plants. The second
category involves surveys of the colour/pattern
polymorphism of populations from different geographic
areas, since adults of the meadow spittlebug exhibit great
colour/pattern variations, both in wing markings and the
colour and pattern of the ventral parts.
In recent decades the meadow spittlebug
P. spumarius
has increasingly become one of the most studied species
on various aspects of biology, since it is very suitable for
genetics, ecology and other population studies. This
review emphasises its importance based on the
information obtained from previous surveys and my own
study.
Ecology
Habitat and host plants
Owing to its highly polyphagous nature and flexibility,
P. spumarius
occurs in most terrestrial habitats (9,10).
Nymphs and adults are found on various plants in habitats
moist enough to provide them with sufficient moisture to
keep them alive, such as meadows, abandoned fields,
waste ground, roadsides, streamsides, also forests,
hayfields, marshlands, parks, gardens and cultivated
fields.
Hundreds of host plants of
P. spumarius
have been
recorded from North America (2,11), New Zealand (12),
Hawaii (13) and Europe (14-18). These plants range
from grasses to trees, including meadow crops, herbs,
thistles, garden plants, shrubs, even conifers.
Dicotyledonous plants tend to be used more often than
monocotyledonous plants (14,17).
Nymphs and adults feed on nearly all parts of the
plants above soil level, but principally on actively growing
parts (e.g., leaves, stems, flowers and fruits) (19,20).
Nitrogen fixing herbaceous legumes and some other
plants which have a high amino acid concentration in the
xylem sap (
Medicago sativa
,
Trifolium
spp.,
Vicia
spp.,
Xanthium strumarium
) are most favoured (21). These
hosts provide a relatively rich source of nitrogen
compounds as nutrition in the xylem (21,22). It has been
pointed out that nitrogen is a limiting factor for some
feeding behaviour in
P. spumarius
(23) and therefore it
may be a selective advantage for individual insects, which
feed on the most nutritious plants.
Geographic distribution and economic importance
It is suggested that humidity is a vital climatic factor
determining the distribution limits of the meadow
spittlebug in all stages of its survival, therefore an
environment that has an abundant water supply for the
plants with high humidity is usually favourable (2).
Although the meadow spittlebug is one of the commonest
insects and has a very wide world distribution, it does not
occur in most arctic, alpine and arid zones, because
temperature is another factor limiting its distribution (9).
For example, the egg hatching and nymphal development
stages of
P. spumarius
are temperature dependent (24),
moreover, adults may die above and below certain
temperature limits (9).
P. spumarius
has been recorded from different
latitudes and altitudes in much of the Palearctic and
Nearctic regions (15,25-27). Its distribution ranges from
north Lapland to the Mediterranean in Europe
(9,10,16,28,). It has been reported from north Africa
(7), several parts of the former Soviet Union (29-32), as
well as Afghanistan (33) and Japan (34). It has been
surveyed in the U.S.A. and Canada where it has been
introduced and is an important pest (2). Its global
distribution also covers the Azores (35), Hawaii and New
Zealand in the Southern Hemisphere where it has been
accidentally introduced in the last few decades
(12,13,17,36,37). Recent records involve Turkey
(38,39,40,41).
On the Polymorphic Meadow Spittlebug,
Philaenus spumarius
(Homoptera: Cercopidae)
448
In Europe,
P. spumarius
is not considered a serious
pest and rarely causes severe damage (42,43). It has
been, however, regarded as an economic pest of crops
and other cultivated plants in America. It mainly causes
two types injury to plants.
The first type of injury is as a vector of some plant
diseases. It has been stated that
P. spumarius
transmits
the virus of PierceÕs disease of grapevines from diseased
to healthy vines and some other plants, which may serve
as reservoirs of the virus (44). It has also been mentioned
that the species may be a vector of peach yellows and
little peach disease, and may be a carrier of the plum mite
(19).
The second type of injury is its directly harmful effect
on plants. The nymphs cause the main injury.
P.
spumarius
nymphs may take up to 280 times their own
fresh weight of the plant sap in 24 hours (22). Heavy
infestations of the nymphs and adults on plants cause
serious damage, leading to reduction and losses in crop
yield.
P. spumarius
is an economically important pest of
alfalfa (
Medicago
sp.) (45-47), goldenrod (
Solidago
sp.)
(48,49), clovers (
Trifolium
spp.) (36), and strawberries
(
Fragaria
spp.) (19,50). Spittlebug injuries weaken the
infested plants and cause significant deformation which
results in delayed plant maturity and reduced forage
yield. Damaged fields give relatively poor second-crop
yield and the effects of the injuries may even persist to
affect yield in the following year.
Population densities of
P. spumarius
may be variable
but often can reach very high densities in suitable
habitats, hence its pest status. Peak densities of 1280
nymphs/m2and 466 adults/m2have been recorded from
some alfalfa fields (20). The same author has also cited
densities of 6680 nymphs per m2. However, the nymphal
densities usually remain under 1000 nymphs/m2and are
rarely recorded over this value in Europe (50).
As a result, it can be said that damage of the meadow
spittlebug to crops and other plants seems quite
significant. However, some of these effects may have
been overestimated. It has been shown that resistant
cultivars to
P. spumarius
can be found in most alfalfas
(51), goldenrods (52) and some other wild and cultivated
plants (53). In addition, effective pesticides and natural
enemies play a significant role in regulating its population
density (19,42,54).
Natural Enemies
Although there is a lack of detailed information
concerning natural enemies, several vertebrates and
invertebrates have been reported to attack adults,
nymphs and eggs of the meadow spittlebug. Harper and
Whittaker (55) released
P. spumarius
specimens after
labelling them with a radioactive isotope and then they
determined the potential predators by scanning their
levels of radioactivity.
Birds are important predators of the meadow
spittlebug. For example, Evans (56) analysed the contents
of the gizzards and faecal pellets of sparrow species
Pooecetes gramineus, Spizella pusilla
and
S. passerina
and
found that their diet contained
P. spumarius
during the
breeding season. Halkka and Kohila (57) summarised a
list of some other common bird predators of the meadow
spittlebug from different authors. These include two
gallinaceous species
Tetrao urogallus
and
Phasianus
colchicus
that appear to feed on the nymphs. Other
species
Perdix perdix, Delichon urbica, Corvus frugilegus,
Turdus viscivorus, T. philomelos, Phylloscopus trochilus
acredula
and
Sturnus vulgaris
in the list are predators of
adults.
The common frog,
Rana temporaria
is another
vertebrate predator of the meadow spittlebug (58). It has
been shown that adult
P. spumarius
appear as the
commonest cercopid in the diet of this frog in Ireland in
September.
Several Arachnids, Hymenoptera, Diptera, and
Coleoptera have been reported as invertebrate predators
of the meadow spittlebug. In particular,
Mitopus morio
and some other spiders have been shown as predators of
adults (55,59). In addition, the prairie ant,
Formica
montana,
has been reported to prey on
P. spumarius
nymphs (60).
P. spumarius
has several parasitic enemies. Adults are
attacked by the dipteran parasitoid
Verralia aucta
(42),
and by the Nematode
Agamermis decaudata
(2).
Furthermore, an entomophagous fungus of the genus
Entomophthora
attacks adults (42). Some Hymenoptera
Ooctonus
spp.,
Tumidiscapus
sp.,
Centrodora
sp. and
dipterans are known as egg parasitoids (2).
Life Cycle
P. spumarius
is known as a univoltine and
hemimetabolous insect in most of its range (61),
although Drosopoulos and Asche (27) believed that the
S. YURTSEVER
449
species may be partly bivoltine in certain parts of Greece.
British and some Turkish
P. spumarius
populations are
univoltine (10,18). After the overwintering, egg hatching
begins in April. There are five nymphal instars and adults
appear in June. Adults start to mate soon after the final
eclosion, and copulating pairs can be seen throughout the
summer. Adults exist at least until October. However, as
the summer season advances the number of males
declines in proportion to females (61), since males
generally do not survive as long as females (10).
Oviposition commences in early September, females are
induced to lay eggs by the short daylight and the low
temperature, and then eggs undergo overwintering
diapause. Before the hatching in spring, this diapause is
broken by exposure to a chill period _which is less than
5¼C _of about 100 days (62).
There are certain temperature thresholds, which play
an important role on the egg hatching and nymphal
developmental stages (24,50), that temperature
influences could modify the egg hatching and
developmental rates of these periods. The low
temperature causes severely delayed development of the
nymphs (63). Development to adulthood requires a sum
of 700-800 day-degrees above 5¼C (9). Hence, in cooler
climatic conditions development to the adult stage takes
longer. Adult mortality, therefore, in such areas begins
earlier owing to frost. Finnish Lapland is the northern
limit of the speciesÕ distribution; nymphs may last up to
mid-August but sometimes are killed by the first autumn
frost (9). In western Turkish populations, adults
disappear earlier than northern European populations,
due to dry summer conditions (Yurtsever, unpublished
data).
Hawaii is the only tropical area where this species is
recorded, but it is restricted to the cooler highland sites
(64,65). In Hawaii, however, there is no clear pattern of
seasonality for the life cycle, since the day-length remains
at about 12 hours throughout the year (13,17). New
Zealand is probably the southern limit of the species.
Accordingly, in New Zealand, the life cycle of the species
has shifted by six months parallel to the seasonality of the
Southern Hemisphere (37).
The phenology of the life cycle of
P. spumarius
may
be different in certain parts of its global distribution,
because the species encounters an extensive range of
climatic conditions due to its wide distribution. However,
variations of the life cycle are not fundamentally different
(2,9,11,17 27,37,42,66). In North Europe, gravid
females begin to lay eggs in late summer. The number of
the eggs laid varies but an individual female may produce
up to 350-400 eggs (67). The eggs are laid in packets
sometimes containing 10-20 eggs held together by frothy
cement. In the laboratory conditions, each nymphal stage
takes about 10 days, and adults usually appear
approximately 50 days after the hatching. The females
may mate a few days after emergence. The life cycle is
completed by the oviposition stage.
Breeding
Philaenus spumarius
in the laboratory
conditions
Owen and Wiegert (68) emphasise that breeding
P.
spumarius
in captivity is difficult although several
attempts have succeeded (2,11,24,63,69). However,
none of them have been performed in real laboratory
conditions. Although these breeding studies have dealt
with different disciplines, very little attention has been
paid to the inheritance of the polymorphism. The majority
of these studies have been concerned with the ecology or
other non-genetical aspects of the polymorphism.
In contrast, Halkka et al. (70) carried out genetical
crossing experiments with Finnish
P. spumarius
in natural
habitat conditions. The first laboratory breeding
experiments on the inheritance of this polymorphism
were carried out with British populations by Stewart and
Lees (71), and laboratory culture techniques have been
described in detail by West and Lees (62). The long life
cycle is one of the difficulties of studying
P. spumarius
.
Nevertheless in certain laboratory regimes the life cycle
may be shortened to six months (71). This is also
confirmed with recent extensive laboratory experiments
(18, 67). Thus, in the laboratory conditions, the life cycle
of
P. spumarius
can be described as follows.
Eggs
These are about 1 mm long, and 0.35 mm wide,
elongated, ovoid and tapering in shape. When first
oviposited, the egg is yellowish white and has a dark
orange pigmented spot in the shell at one end. If the egg
is fertilised this orange spot gets bigger and a black
coloured, lid-like formation develops on it in about 90
days (67). This lid-like black formation clearly indicates
that the eggs are ready for hatching. The young nymph
leaves the egg through the black lid. The black lid does
not develop if the egg is not fertilised or if it is unhealthy;
the orange spot still remains but the egg turns brown and
eventually shrivels. In optimum conditions, hatching takes
On the Polymorphic Meadow Spittlebug,
Philaenus spumarius
(Homoptera: Cercopidae)
450
place after approximately 20 days and the first instar
appears.
Nymphs
There are five nymphal instars. The first instar is light
orange when newly emerged. This orange colour
gradually turns green from the late first instar to the fifth
instar. As the nymph develops some other morphological
changes occur also. For example, the body length
increases through successive instars and the length of the
legs gets longer in proportion to the body length, the
abdomen flattens dorso-ventrally. Also wing pads begin
to appear in the third instar and they become more visible
in the fourth and the fifth instars. In this way, different
stage nymphs can be distinguished morphologically from
each other. In addition, the fourth and the fifth instars
are detected by the larger spittle masses they produce on
the host plant. The fourth and the fifth instars may be
sexed according to their nymphal external genitalia.
The first instar
The body length is approximately 1.35 mm, when
freshly hatched. It is orange and produces little spittle on
the host plant. Wing pads and external genitalia are not
developed. It is very delicate, and moves slowly.
The second instar
The body length is approximately 2.25 mm and
slightly bigger than the first instar, but they can be
distinguished from them by their yellowish orange colour.
Wing pads and external genitalia are still not developed.
The third instar
The body length is approximately 3 mm and more
greenish than yellow. It is clearly distinguishable from the
previous instars. In addition, wing pads and external
genitalia begin to develop, but still the nymphs cannot be
sexed.
The fourth instar
The body length is approximately 4.75 mm and
green. Yellowish wing pads are clearly visible and,
external genitalia are developed. The fourth instar can be
sexed with difficulty under ca x10 magnification.
The fifth instar
The body length is approximately 6.25 mm and
green. Yellowish wing pads are well developed, external
genitalia can clearly be seen under magnification. They
produce a great deal of spittle on the host plant.
Adults
The body length is approximately 6 mm, females are
slightly larger than males. In the laboratory conditions,
adults emerge approximately 50 days after nymphal
stages. Adults usually stay in the spittle mass until the
cuticle is hard and fully pigmented. However, they may
occasionally leave their spittle mass earlier. Adults are
fully mature approximately ten days after leaving the
spittle and females may mate several times thereafter.
The colour/pattern polymorphism
The dorsal colour/pattern polymorphism
Adults of
P. spumarius
are polymorphic for dorsal
colour/pattern throughout the speciesÕ range. There is
great variation in wing markings. This caused the morphs
of
P. spumarius
to be given species status by many earlier
authors. More than sixty synonyms have been given to
the species due to its colour variation (2). In addition,
some morphs have been given subspecies status (72).
Numerous varietal names have been listed concerning the
morph differences (44,73-75). Many different names
have been given to the same colour forms. Consequently,
these have caused confusion in the nomenclature. The
meadow spittlebug was commonly called
Philaenus
leucophtalmus
in the early literature. However,
Ossiannilsson (76) stated that the name
P. spumarius
was
consistent with the original intention of Linnaeus and the
International Commission of Zoological Nomenclature in
1961 decided on the valid specific name as spumarius
(77).
The dorsal colour/pattern variation of the meadow
spittlebug has attracted many researchers in ecological
and genetical studies. Classifications of the phenotypes
have been made by several authors (29,31,34,61,77-
80). The number of colour/pattern phenotypes has been
the source of some debate (15,25, 30,74,81-83).
Initially, nine phenotypes were determined, then, Stewart
and Lees (10) suggested that there are thirteen main
colour phenotypes. According to my extensive literature
survey in the present paper, 16 phenotypes are found in
many natural populations (Fig. 1).
Inheritance of eleven commonly occurring colour
phenotypes has been studied extensively (41,70,71).
These colour phenotypes are clearly inherited and are
referred to by three-letter abbreviations for convenience,
as follows:
populi
(POP),
typicus
(TYP),
trilineatus
(TRI),
marginellus
(MAR),
lateralis
(LAT),
flavicollis
(FLA),
S. YURTSEVER
451
gibbus
(GIB),
leucocephalus
(LCE),
quadrimaculatus
(QUA),
albomaculatus
(ALB), and
leucophtalmus
(LOP).
The first three are essentially very pale brown (golden)
with darker mottling or stripes (the non-melanics) and
the remaining are predominantly black or dark brown
with pale markings in various combinations on the vertex,
pronotum and wing patterns (the melanics). The other
phenotypes:
vittatus
(VIT),
marginellus/flavicollis
(MAR/FLA),
ustulata
(UST),
praeusta
(PRA), and
hexamaculata
(HEX) rarely occur in different natural
populations (10,26,30,39,73,81,83,84).
In some populations, certain phenotypes, particularly
dorsal melanics are not expressed in males as clearly as in
females, for exam
ple, in Finnish populations melanics
seem to be limited to females (81). In British populations
from south Wales there is no obvious differences between
the sexes in overall melanic frequency (71). Large
population samples from all over Turkey do not indicate
any sex limitation, but significant phenotype variations
occur between certain populations (Yurtsever and
Zeybekoglu, unpublished data).
The genetic basis of the dorsal colour/pattern
polymorphism
The dorsal colour/pattern polymorphism is determined
by seven alleles at a single locus with complex dominance
and co-dominance relationships (Fig. 2). Eleven principal
phenotypes can be divided into groups as melanics and
non-melanics (Fig. 1) (10). One of the three non-melanic
phenotypes, TRI, is controlled by the allele ÔTÕ, the other
non-melanics POP and TYP are controlled by the same
allele ÔtÕ. The two main melanic groups (FLA) + (GIB) +
(LCE) and (QUA) + (ALB) + (LOP) are controlled by one
allele each at the main colour locus, the alleles ÔCÕ and ÔOÕ
respectively (70, 71). Another non-melanic phenotype,
VIT, is also thought to be controlled by the allele ÔTÕ (10).
On the other hand, there is another allele ÔFÕ which is
responsible for producing the FLA phenotype alone.
Hence, the phenotype FLA is an expression either of the
allele ÔCÕ or ÔFÕ. Moreover, two other melanics, MAR and
LAT, are controlled by the alleles ÔMÕ and ÔLÕ respectively.
Some of the white head/elytral patterns are co-dominant.
For example, MAR can also be expressed in the
heterozygote condition by the combinations of the alleles
L/C and L/F (Fig. 1). The alleles producing white patterns
in head/elytral margins are dominant over the alleles
responsible for dark pigmentation in corresponding parts
(9). Furthermore, there may be some other non-allelic loci
or locus responsible for the regulation of the phenotypic
variation within each group (85).
The genetic basis of the rare phenotypes mentioned
before is not very clear. Thompson and Halkka (83) point
out that the UST appears to be a variant within the
populi-typica complex. VIT and PRA are often considered
minor modifications of TRI (33,73,83), but Stewart and
Lees (10) have regarded them separately from TRI and
they suggested that VIT is variety of TRI. However, none
of these authors presented inheritance data. Based the
laboratory data, Yurtsever (67) proposed that VIT is a
variety of TRI and suggested that HEX, PRA and UST are
expressed by different alleles.
On the Polymorphic Meadow Spittlebug,
Philaenus spumarius
(Homoptera: Cercopidae)
452
Figure 1. The 16 dorsal phenotypes of
Philaenus spumarius
occurring in many natural populations. The top row, the
non-melanics, from left to right are: POP, TYP, TRI. The
bottom row, the rare phenotypes are: VIT, MAR/FLA, PRA,
UST, HEX. The remaining are melanics. The second row:
MAR, LAT. The third row: FLA, GIB, LCE. The fourth row:
QUA, ALB, LOP. Full names of the phenotypes are given in
the text.
The dominance hierarchy models of common eleven
phenotypes for the two regions, Fennoscandia and south
Wales urban are well known. Halkka et al. (70) have
demonstrated that the dominance relationships in
Fennoscandian populations are different in the two sexes.
Accordingly, in both sexes the allele TRI is top dominant
but in males POP/TYP are dominant to the melanics
whereas in females the melanics occupy the second place
after the allele TRI, followed by POP/TYP in the
hierarchy. However, Stewart and Lees (71) have found
no different pattern of dominance in the two sexes, TRI
is again top dominant followed by the melanics then
POP/TYP are bottom recessive in males as well as in
females. They have also found reversal of dominance
between the alleles MAR and FLA-F concerning the sexes.
Their breeding experiments reveal that MAR is dominant
over FLA-F in females, conversely MAR is recessive in
males (Fig. 2). The dominance hierarchy between the
phenotypic groups can be summarised as in Figure 2.
In New Zealand populations, only two phenotypes,
FLA and TYP, occur (37) and FLA is dominant over TYP
in both sexes (41). The model of inheritance in a rural
Welsh (Llysdinam) population (67) is slightly different
from two previous studies involving Fennoscandian and
urban Welsh (Cynon Valley) populations. The Llysdinam
model fundamentally follows the Cynon Valley model but
differs in the inheritance of MAR. Because in the
Llysdinam population, MAR is to be found dominant over
TYP in females but recessive in males similar to the
Finnish model, but the dominance hierarchy of the other
phenotypes is the same as in the Cynon Valley model. The
Llysdinam model is supported by the more restricted
investigation of the Skokholm, west Wales (67) and
Turkish populations (18). Although some authors
suggested that FLA and LAT are co-dominant with each
other (10,70), they presented no data confirming their
reports. Nevertheless, Yurtsever (67) found clear
experimental evidence supporting their suggestions.
Geographic variation of dorsal colour/pattern
phenotypes
The occurrence and frequencies of the dorsal
colour/pattern phenotypes vary from location to location.
Several selective influences associated with the
environmental factors have been suggested (26).
Patterns of variation may be affected by the habitat
composition (86). Variation in morph frequencies may
even occur within one habitat at the subniche level is
associated with the host plant types. Geographic variation
in morph frequencies across Europe is parallel to
changing climatic conditions (81,87). From North
American populations eight phenotypes, whereas from
Italian populations fifteen phenotypes have been
recorded. Although
P. spumarius
has been recorded from
several parts of Turkey (38,40), there is very limited
information about morph variations (18,39).
The large scale geographic variation indicates that
most melanics with some exceptions are increased in
frequency from south to north in some American and
European populations (82,88). The latitude is associated
with morph frequency variation (26,28). Increasing
S. YURTSEVER
453
p
M
p
T
p
F
p
C
p
L
p
O
p
t
females
males
Figure 2. Dominance hierarchy for the 11 common phenotypes of
Philaenus spumarius
in some British populations. Arrows
show direction of dominance and double lines show co-
dominance. The p donates pigmentation locus ÒpÓ for seven
alleles. Each phenotype in the figure represents its own
phenotypic group as described in the text. (After Stewart
and Lees 1996).
melanic frequencies are positively correlated with altitude
(15,32). Accordingly, Thompson (82,88) proposed that
the high melanic frequency association with the cooler
climates is a consequence of thermal selection. Consistent
with the hypothesis, Berry and Willmer (89)
experimentally verified that thermal melanism is possible.
Studies on British populations have shown that
industrial melanism occurs in
P. spumarius
(90). There is
a strong association between the high melanic frequencies
and intense atmospheric pollution in some urban areas
where industrial pollution has occurred (91,92). In
contrast, no association is found between melanic
frequencies and degree of pollution in industrial areas in
Chicago and Czechoslovakia (83,93), respectively.
Although
P. spumarius
populations show industrial
melanism, the selective mechanisms are not clearly
known which are responsible for maintaining this
polymorphism. The associations may be climatic with
colour and pattern functioning as an important
thermoregulatory component. However, the effects of
predation and the other direct effects of air pollution
cannot be ruled out (90).
The importance of the predation is also known in the
polymorphism of
P. spumarius
, this is probably one of the
selective forces influencing the polymorphism
(42,94,95). Birds are presumably the most likely
predators serving for apostatic selection (1,96). In
addition to the deterministic influences discussed, the
stochastic effects have also been shown in some island
populations in the Finnish Baltic (85,97-99). These
studies have demonstrated that low variability and morph
frequency differentiation on the small isolated island
populations were due to genetic drift. The presence of
only two of the eleven phenotypes in New Zealand and
Hawaii populations are consistent with loss of genetic
variation due to the founder effect (9, 37).
The ventral colour/pattern variation
As with its dorsal colour/pattern polymorphism, the
meadow spittlebug
P. spumarius
, exhibits remarkable
variation on the ventral surface. Although there are
records from East European, Russian (30,84), Finnish
(100) and North American (88) populations dealing with
ventral variation in
P. spumarius
, virtually no detailed
work had been done until recently (67,101).
West (101) surveyed several populations of
P.
spumarius
in England and Wales and found variation from
very dark to light on the ventral surface. He analysed 18
characters of the ventral surface according to their
darkness level. This revealed that the darkness on the
ventral surface is associated with the dorsal phenotype.
West (101) also demonstrated the influences of sex and
location on ventral darkness. Detailed laboratory studies
demonstrated that the ventral darkness of certain TRI
phenotypes is associated with its genotype (67,101).
That is, dark ventral TRIs are heterozygous for a dorsal
melanic phenotype and light ventral TRIs are
heterozygous for POP or TYP.
Svala and Halkka (100) have shown clinal variation in
the patterning of the frontoclypeus in females from
several Finnish populations and have suggested that the
frons patterning differs between the sexes. Beregovoi
(84) reports that the sexes show differentiation on the
frons and pleurites with regard to pigmentation. His
study reveals that the frequency of
P. spumarius
males
with dark pleurites increases from south to north in
Russian populations. In North America, a similar
increased frequency of dark pleurites in males towards
the north and cooler temperatures is found (88). Striking
variation in the frontoclypeal patterning also occurs in
several British populations (101).
Svala and Halkka (100) mentioned that pigmentation
on the frontoclypeus is genetically determined, though
they provided no evidence from crossing experiments
supporting this assumption. West (101) suggests that
ventral darkness in
P. spumarius
is discontinuous, and is
under genetic control, and the same colour locus
responsible for dorsal melanism possibly controls
pigmentation on the ventral surface. Parallel to those
suggestions, recent experimental evidence confirms that
ventral darkness in
P. spumarius
is a heritable trait (67).
Interestingly, certain British and Turkish populations
show significant differences in the ventral darkness (67).
This is probably due to different selection regimes that
the populations are responding to.
Polyandrous aspect of
Philaenus spumarius
This striking aspect of the meadow spittlebug was just
recently reported (102). The female
P. spumarius
may
copulate several times with different males during the
reproductive period of the life span. Consequently,
different males may father the offspring of the same
female. Multiple mating does not influence the number of
the progeny, but it may provide great genetic and thus
evolutionary benefits to the meadow spittlebug as
reported in many polyandrous species (103-106).
On the Polymorphic Meadow Spittlebug,
Philaenus spumarius
(Homoptera: Cercopidae)
454
Discussion
The studies with
P. spumarius
reveal that the dorsal
colour/pattern polymorphism occurs throughout its
extensive range. These include small isolated island
populations (97,99) and even localised populations in
fine-grained environments as in the examples of the areas
which are exposed to intense particulate air pollution the
Cynon Valley (91) and the Cardiff Docks (92). Although
the occurrence and frequency of the phenotypes vary in
different environments (9,10,37,90) no populations have
yet been found with a fixed allele.
The general applicability of the inheritance of dorsal
colour/pattern polymorphism emerging from previous
studies is supported with the material from rural
populations of Britain, New Zealand, and Turkey. In
addition to seven alleles of dorsal polymorphism, it
appears that there may be another allele controlling the
expression of the phenotypes UST (
ustulata
) and HEX
(
hexamaculata
), but this is not conclusive at present.
Halkka et al. (87) reported that there might be two other
alleles, the ÔVÕ and ÔPÕ responsible for the VIT (
vittatus
)
and PRA (
praeusta
) phenotypes respectively. However,
there is no sign of an independent allele for VIT (67), and
this phenotype appears to be a variety of TRI, in
agreement with previous suggestions (10). The position
of PRA in this polymorphism is still unclear.
Some of the subtle differences in the inheritance of
the dorsal colour/pattern polymorphism in
P. spumarius
between the areas studied may be related to local
conditions acting as a selective effect on this
polymorphism. The melanic forms may be more resistant
to the influences of the effects of particulate or gaseous
pollution in the polluted areas (91). Accordingly, the local
environmental influences may be important for certain
phenotypes in a given area. Thus, these conditions may
provide some advantages to them over other phenotypes
resulting in fitness, such as more efficiently evading
predators, finding a mate and food resources (91).
Natural selection probably exerts its influence in the
form of climatic selection (97). The importance of
apostatic selection responsible for the variety and
maintenance of the dorsal colour pattern polymorphism is
emphasised (68). Thompson (94) argues that the
apostatic selection hypothesis does not explain evolution
of geographic variation, and particularly clinal variation.
Nevertheless the MAR phenotype occurs, at a higher
frequency than other melanic forms in certain parts of
North America (83), and this is attributed to aposematic
selection (94,107). According to Thompson (94), black
and white pigmentation of the MAR phenotype (in
females) represents an example of escape warning
coloration, and the pattern of this phenotype mimics
avian excrement. Therefore, experienced predators
ignore MAR individuals because they remember previous
frustrating attempts with this similar pattern that they
have encountered. However, experimental evidence for
this hypothesis is lacking.
Owen (108) represents examples of similar
polymorphisms in
P. spumarius
and the land snail,
Limicolaria martensiana
that are exposed to similar
pattern selection. The colour pattern of the shell in the
snail
L. martensiana
is extremely variable and the species
is locally very abundant, occurring in high densities. The
four shell forms in coloration apparently resemble dorsal
phenotypes of
P. spumarius
(TYP, TRI, MAR, POP). The
relative frequencies of the four forms of
P. spumarius
in
an alfalfa field in Michigan and of the forms of
L.
martensia
in a eucalyptus plantation near Kampala are
parallel to each other. Relative frequencies of the colour
forms in these two species are determined by apostatic
selection, because the forms concerned are apparently
cryptic and may be at a selective advantage over the non-
cryptic forms.
In some circumstances, morph frequencies in natural
populations of
P. spumarius
may reflect stochastic events
(85,97-99) despite the view that all genetic
polymorphisms are maintained, and morph frequencies
determined by natural selection (109).
The mode of inheritance of this polymorphism in this
species is simply governed by a one-locus system as is
often observed in many arthropod species concerning
melanism. However, the role of the modifier genes in the
polymorhism of
P. spumarius
must be borne in mind
(110), because observed genetic differences between
various populations of a polymorphic species may not be
only for the primary genes for melanic patterns but for
their modifiers as well. The role of modifiers affecting the
expression of the colour locus in many natural
populations is now well understood (111,112). The
studies with
P. spumarius
show another way in which the
genetic architecture of natural populations could be
changed by modifiers.
S. YURTSEVER
455
The influence of selective factors in ventral darkness is
unknown. The differential ventral darkness variation in the
meadow spittlebugs between Turkey and Britain is striking
(67). British
P. spumarius
populations do not manifest
geographic pattern in certain ventral parts (101). However,
in some natural populations, ventral surface may respond to
selection as the dorsal surface in certain environments.
Moreover, some kind of non-visual selection may influence
phenotype frequencies (91,92,113,). Variation in the
populations concerned on a large geographic scale may be
evident (30,88) and differences can be expected between
widely separated populations concerning this particular
character (84,100).
Multiple paternity is probably a novel aspect in
P.
spumarius
and would repay future study. Although
information is limited for the incidence of multiple mating
in the wild, it does occur in natural populations (102).
Since this homopteran insect shows very high habitat
diversity (10), multiple mating is probably one of the
leading reasons of the species occupying numerous
terrestrial habitats in many regions of the world, because
multiple mating provides many evolutionary advantages
to polyandrous species through increased genetic
variability and high fitness (104-106).
On the Polymorphic Meadow Spittlebug,
Philaenus spumarius
(Homoptera: Cercopidae)
456
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... the presence of the foam within which the nymphs develop and whose role is to protect them 468 against such dangers (Yurtsever, 2000b). Nymphs could also be killed by herbivorous mammals 469 during their food intake, although this scenario is unlikely as Cistus ssp. ...
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