Distribution of common genotypes of Myzus persicae (Hemiptera : Aphididae) in Greece, in relation to life cycle and host plant

Department of Entomology, The Natural History Museum, London, SW7 5BD, UK.
Bulletin of Entomological Research (Impact Factor: 1.91). 07/2007; 97(3):253-63. DOI: 10.1017/S0007485307004907
Source: PubMed
Microsatellite genotyping was used to identify common clones in populations of the Myzus persicae group from various hosts and regions in mainland Greece and southern Italy and to compare their distribution and occurrence on tobacco and other crops. Common clones were defined as genotypes collected at more than one time or in more than one population; and, therefore, unlikely to be participating in the annual sexual phase on peach. Sixteen common genotypes were found, accounting for 49.0% of the 482 clonal lineages examined. Eight of these genotypes were subjected, in the laboratory, to short days and found to continue parthenogenetic reproduction, i.e. they were anholocyclic. Four of the six commonest genotypes were red, and one of these accounted for 29.6% of the samples from tobacco and 29.4% of those from overwintering populations on weeds. All six commonest genotypes were found on weeds and five of them both on tobacco and on other field crops. In mainland Greece, the distribution of common clones corresponded closely with that of anholocyclic lineages reported in a previous study of life cycle variation. Common genotypes were in the minority in the commercial peach-growing areas in the north, except on weeds in winter and in tobacco seedbeds in early spring, but predominated further south, away from peach trees. This contrasts with the situation in southern Italy, reported in a previous paper, where peaches were available for the sexual phase, yet all samples from tobacco were of common genotypes.


Available from: JOHN A. TSITSIPIS, Jun 17, 2014
Distribution of common genotypes
of Myzus persicae (Hemiptera: Aphididae)
in Greece, in relation to life cycle
and host plant
R.L. Blackman
, G. Malarky
, J.T. Margaritopoulos
and J.A. Tsitsipis
Department of Entomology, The Natural History Museum, London,
SW7 5BD, UK:
Laboratory of Entomology and Agricultural Zoology,
Department of Agriculture Crop Production and Rural Environment,
University of Thessaly, Fytokou Street, 384 46 Nea Ionia, Magnesia, Greece
Microsatellite genotyping was used to identify common clones in populations of
the Myzus persicae group from various hosts and regions in mainland Greece and
southern Italy and to compare their distribution and occurrence on tobacco and
other crops. Common clones were defined as genotypes collected at more than one
time or in more than one population; and, therefore, unlikely to be participating in
the annual sexual phase on peach. Sixteen common genotypes were found,
accounting for 49.0% of the 482 clonal lineages examined. Eight of these geno-
types were subjected, in the laboratory, to short days and found to continue
parthenogenetic reproduction, i.e. they were anholocyclic. Four of the six
commonest genotypes were red, and one of these accounted for 29.6% of the
samples from tobacco and 29.4% of those from overwintering populations on
weeds. All six commonest genotypes were found on weeds and five of them both
on tobacco and on other field crops. In mainland Greece, the distribution of
common clones corresponded closely with that of anholocyclic lineages reported in
a previous study of life cycle variation. Common genotypes were in the minority
in the commercial peach-growing areas in the north, except on weeds in winter
and in tobacco seedbeds in early spring, but predominated further south, away
from peach trees. This contrasts with the situation in southern Italy, reported in a
previous paper, where peaches were available for the sexual phase, yet all samples
from tobacco were of common genotypes.
Keywords: cyclical parthenogenesis, life cycle variation, clones, Myzus persicae
nicotianae, tobacco aphid
Studies of the population genetics of aphids are compli-
cated by their cyclical parthenogenesis. In a typical aphid
annual life cycle (a holocycle), a bisexual generation through
the winter alternates with a succession of parthenogenetic,
all-female generations (clones) through the spring and
summer. In some common pest aphid species such as Myzus
persicae (Sulzer) (Hemiptera: Aphididae), life cycle variability
introduces additional complicating factors. Some lineages
have completely or partially lost the bisexual generation and
overwinter anholocyclically, either reproducing exclusively
by parthenogenesis or contributing only few males (andro-
cyclic genotypes) and/or few mating females (intermediate
Fax: 020 7942 5229
E-mail: r.blackman@nhm.ac.uk
Bulletin of Entomological Research (2007) 97, 253–263 doi:10.1017/S0007485307004907
Page 1
genotypes) to the sexual phase (Blackman, 1971, 1972). Also,
M. persicae is one of many aphid species undergoing annual
host alternation, so that the sexual phase occurs on a woody
host plant, the peach Prunus persica L. (Rosaceae), that is
totally unrelated to the herbaceous host plants of the
parthenogenetic phase.
Thus, the winged parthenogenetic females of M. persicae
that fly in and establish populations on field crops in spring
and summer can come from two different sources, which
have very different effects on the genetic structure of the
population. A population of M. persicae on a crop in summer
can consist of a mixture of clones, and some of these may be
new recombinants that have migrated from peach in the
spring, while others may be old lineages that came through
the previous winter(s) in the parthenogenetic phase on
herbaceous plants. The proportions of new and old clones
will depend on (i) the availability of peach trees for the
sexual phase (Margaritopoulos et al., 2002) and (ii) the
suitability of the climate for overwintering in the partheno-
genetic phase (Blackman, 1974). The analysis and interpreta-
tion of genetic data has to take full account of the interacting
effects of life cycle category, climate and host plant, if it is to
provide any realistic assessment of the extent of genetic
differentiation and gene flow between populations.
The genetic structure of populations of M. persicae in
mainland Greece is of particular interest for two reasons. The
first concerns the life cycle variation. There are highly signifi-
cant differences in the proportions of the different life cycle
categories between regions. Margaritopoulos et al. (2002)
tested the life cycle categories of clonal lineages established
from field populations sampled in spring and summer by
subjecting them to short photoperiod and reduced tempera-
ture in the laboratory. Most clones established from aphids
collected within peach-growing regions responded to these
conditions by producing a bisexual generation, whereas
most of the clones from north-eastern, southern and central
areas, away from peach-growing regions, continued
parthenogenetic reproduction, i.e. in the field they would
be destined to overwinter anholocyclically. It was, therefore,
of interest to determine the extent to which the genetic
structure of populations reflected these regional differences.
Microsatellite DNA or allozyme markers have been used
to provide information on the relationship between life cycle
category and genotypic structuring of European populations
of the aphid species, Sitobion avenae (Fabricius) (Simon et al.,
1999) and Rhopalosiphum padi (Linnaeus) (Delmotte et al.,
2002). In microsatellite DNA studies of M. persicae, Wilson
et al. (2002) found that populations with a sexual phase from
different localities in south-east Australia, mostly sampled
from peach, generally conformed to Hardy-Weinberg equili-
bria, had high clonal diversity and showed significant
population differentiation. In another study also involving
M. persicae lineages from Australia (Victoria), but from
herbaceous hosts (Vorburger et al., 2003), both winter tem-
perature and availability of peach trees were found to affect
the geographical distribution of genotypes of different life
cycle category, clonal diversity being highest in populations
with a sexual phase. Furthermore, Guillemaud et al. (2003)
reported that the mode of reproduction of M. persicae in
France affected genotypic variability, populations with a
bisexual generation being far more variable than those that
overwintered parthenogenetically.
The second reason for a particular interest in Greek
M. persicae is that their morphology shows significant
differences between regions and, in particular, according
to the secondary host plant (Margaritopoulos et al., 2000).
Multivariate morphometric analysis was performed on
clones reared under controlled conditions on the same host
plant, indicating that these differences have a genetic basis.
Clones originating from tobacco Nicotiana tabacum L.
(Solanaceae), and from peach in tobacco-growing regions,
differed in morphology from clones collected from other
secondary host plants, and from peach away from tobacco-
growing regions, and clustered together in spite of regional
differences. These results confirmed those of previous
studies (Blackman, 1987; Blackman & Spence, 1992), on
samples from tobacco and other plants from many parts of
the world, indicating the existence of a closely related, but
nevertheless genetically distinct, tobacco-adapted form, for
which Blackman (1987) proposed the name Myzus nicotianae
Blackman. The identical DNA sequence at some loci
examined (Field et al., 1994; Clements et al., 2000a), however,
suggested that some interbreeding must occur. Recently,
subspecific status, Myzus persicae nicotianae Blackman
(Margaritopoulos et al., 2003; Eastop & Blackman, 2005), has
been proposed for the tobacco-feeding form. It has been
proved that adaptation to tobacco involves negative trade-
offs that reduce the fitness of tobacco aphids on other crops
(Nikolakakis et al., 2003) and, along with selection against
host migrants, promoted the evolution of an improved host-
recognition mechanism in winged migrants (Margarito-
poulos et al., 2005; Troncoso et al., 2005).
DNA studies on M. persicae, including some aimed
specifically at comparing tobacco- and non-tobacco-feeding
populations, have failed to find consistent diagnostic genetic
markers (Fenton et al., 1998; Margaritopoulos et al., 1998;
Clements et al., 2000a,b; Zitoudi et al., 2001). However, apart
from the work by Terradot et al. (1999), which included only
two clones from tobacco, there have as yet been no com-
parative studies of tobacco- and non-tobacco-adapted forms
using microsatellite markers, which are currently the most
suitable markers for population genetic analysis. Such
studies need to take full account of life cycle category, so
as to be able to concentrate on the genotypes that are likely to
be participating in sexual reproduction and can, therefore, be
used to estimate the genetic differentiation between popu-
lations and the extent of gene flow.
Using microsatellites, we have genotyped clonal samples
of M. persicae group aphids collected in different regions of
Greece on both primary and secondary host plants and in one
region in southern Italy. In the present paper, we examine
the number and distribution of common genotypes, i.e.
those found at more than one time and/or in more than
one population, in relation to host plant and regional life
cycle variation. These common genotypes are assumed not to
be contributing, or to be contributing only irregularly, to the
sexual phase on peach. We test this assumption by examining
the life cycle traits of the most commonly occurring geno-
types. In another paper (Margaritopoulos et al., 2007),
we analyse and compare genotypes that are unique to
single populations, and which are, therefore, regarded as
contributors to the sexual phase.
Materials and methods
Aphid sampling
Samples of M. persicae group aphids were collected from
peach, tobacco, pepper Capsicum annuum L. (Solanaceae),
R.L. Blackman et al.
Page 2
potato Solanum tuberosum L. (Solanaceae), cabbage Brassica
oleracea L. (Brassicaceae) and various weeds, such as
shepherd’s purse Capsella bursa-pastoris (L.) (Brassicaceae),
whitetop Cardaria draba (L.) (Brassicaceae) and common
mallow Malva sylvestris L. (Malvaceae), in different regions
of mainland Greece during 1997–2000 (fig. 1). Samples were
collected from tobacco-growing areas, except for those from
the east-central coastal area near Volos, which is about
100 km from the nearest tobacco fields. In addition, samples
were collected from tobacco fields in the region of Caserta
(near Naples) in southern Italy in 1998. Samples of two to
three leaves infested by aphids from single plants were
placed in polybags and taken back to the laboratory, where
clonal lineages were initiated from one aphid from each
polybag, by isolation on an excised potato leaf in a Blackman
box (Blackman, 1971). When population sizes were large on
peach and tobacco, a method of systematic sampling was
used. In tobacco fields, plants were sampled every 4–5 rows
and at approximately every 5 m in the row. In peach
orchards, samples were taken every 4–5 trees in the row.
On other field crops, and in the case of overwintering
populations on weeds, numbers were usually too low or too
irregularly distributed for systematic sampling, but all
samples came from separate plants.
Microsatellite genotypes were obtained for 482 clonal
lineages (table 1). Samples of each lineage were kept at
C. Before freezing, the colour of each lineage was
recorded, and 1–2 individuals were karyotyped for presence
or absence of the common A1,3 translocation that is
associated with esterase 4-based resistance (Blackman et al.,
1978). The responses of a subset of lineages to a short-day
regime (10 h light: 14 h dark at 17
C) were tested to
determine life cycle category (Margaritopoulos et al., 2002,
2003). Clonal lineages were classified as either holocyclic
Southern Italy
Fig. 1. Collection sites of Myzus persicae in mainland Greece and southern Italy (1, Xanthi; 2, Arethousa; 3, Aridea; 4, Alexandria and
Meliki; 5, Ptolemaida; 6, Katerini; 7, Velestino, Volos and Lethonia; 8, Karditsa and Anavra; 9, Amfiklia; 10, Caserta, Salerno and Pisani)
and percentages of the different genotypes found on summer host plants in each region. Charts with three pie segments show
percentages of: (i) common genotypes, i.e. collected at more than one time and place (black area); (ii) genotypes collected multiply, but in
a single locality (grey area); and (iii) unique genotypes, i.e. found only one time (white area). Charts with two pie segments show
percentages of anholocyclic and genotypes with a sexual phase (black and white area, respectively).
Population structure of Myzus persicae
Page 3
(responding by producing exclusively males and mating
females and, therefore, destined to have an obligatory
bisexual generation on peach), or anholocyclic (used here
in a broad sense to include all lineages continuing to re-
produce parthenogenetically in a short-day regime and,
therefore, capable of anholocyclic overwintering, although
including some lineages that are able to produce a few males
and/or mating females). Some lineages were tested for
polymorphism at the glutamate oxaloacetate transaminase-1
(GOT-1) locus using a previously-described method
(Blackman & Spence, 1992).
Microsatellite analysis
Seven polymorphic microsatellite loci were used in this
study. Three, M35, M37 and M40, were previously isolated
from an Australian clonal lineage of M. persicae (for primer
sequences, see: Sloane et al., 2001). The additional four loci,
myz2, myz3, myz9 and myz25, were isolated by Gavin
Malarky from a British clone of M. persicae. These four loci
have been used in previous M. persicae studies (Sloane et al.,
2001; Hales et al., 2002a,b; Wilson et al., 2002; Fuentes-
Contreras et al., 2004). Their primer sequences were
published in Wilson et al. (2004). Previous studies have
shown that these loci have sufficient resolution to identify
clonal genotypes (Wilson et al., 2002).
DNA from individual aphids from each lineage was
extracted using a salting-out method (Sunnucks & Hales,
1996), and dissolved in 50 mlofdH
O. Microsatellite
amplification was done using fluorescent-labelled forward
primers from PE-Applied Biosystems UK. The 40 ml reaction
mix contained 1.5 ml DNA, 1.25 units AmpliTaq Gold (Perkin
Table 1. Collection data for samples, colour and karyotype of the 482 clones (n)ofMyzus persicae genotyped.
Region Locality Date Host plant n Red (%) A1,3 (%)
N Aridea Apr–May 98 Peach 7 14.3 0.0 48
Katerini Apr–May 98 Peach 9 22.2 0.0
Meliki Apr–May 98 Peach 10 50.0 0.0
Meliki May 99 Peach 22 18.2 13.6
N Katerini Jun 98 Tobacco 21 33.3 19.0 76
Meliki Jun–Aug 98 Tobacco 33 18.2 6.1
Meliki Jun 99 Tobacco 22 36.4 14.3 (1)
N Katerini May 98 Seedbed 13 30.8 16.7 (1) 14
Meliki May 99 Seedbed 1 0.0 0.0
N Katerini Aug 98 Pepper 2 0 0.0 44
Meliki Aug 98 Cabbage 15 60.0 60.0
Meliki Jun 98 Pepper 3 0.0 33.3
Meliki Jun 99 Pepper 4 25.0 0.0
Meliki Jun–Aug 99 Potato 10 0.0 0.0
Ptolemaida Aug 98 Pepper 10 20.0 20.0
N Katerini Mar 98 Cardaria 7 0.0 0.0 27
Katerini Mar 98 Malva 3 0.0 0.0
Katerini Feb–Apr 99 Capsella 8 0.0 0.0
Katerini Feb 99 ‘Weeds’ 9 66.7 62.5 (1)
NE Xanthi Jun 99 Tobacco 20 90.0 10.0 20
NE Xanthi Jun 99 Pepper 9 66.7 0.0 9
C Karditsa Jun–Aug 98 Tobacco 33 81.8 69.7 33
C Karditsa May–Jun 98 Seedbed 40 75.0 57.5 40
C Karditsa Jun–Aug 98 Pepper 26 42.3 30.8 (1) 26
C Karditsa Jan–Feb 98 Capsella 20 95.0 65.0 21
Karditsa Jan 99 Capsella 1 100 100
EC Lehonia May 98 Peach 13 0.0 0.0 26
Lehonia May 00 Peach 13 0.0
EC Lehonia Jun 99 Pepper 12 8.3 16.7 14
Volos Aug 98 Pepper 2 0 0.0
S Amfiklia Jul 98 Tobacco 19 89.5 72.2 (1) 19
S Amfiklia Aug 98 Pepper 1 100 11
Amfiklia Jul 99 Pepper 10 90 50.0
S Amfiklia Jan 98 Capsella, Sonchus 2 100 100 3
Amfiklia Mar 99 Capsella 1 100 100
SI Caserta Jul 98 Tobacco 38 97.4 91.9 (1) 44
Scafati Jul 98 Tobacco 6 100 100
S Pisani Aug 98 Broccoli 7 57.1 57.1 7
Clones with A1,3 translocation. In brackets, number of clones not karyotyped.
N, NE, C, EC and S are north, north-east, central, east-central and southern mainland Greece, respectively; SI, southern Italy; seedbed,
tobacco seedbed.
R.L. Blackman et al.
Page 4
Elmer), 1.5 mM MgCl
-free buffer, 170 mM of each
dNTP and 0.2 m
M forward and reverse primers. The mix was
overlaid with a drop of oil. Amplification was carried out
using the following cycling conditions in a Hybaid PCR
machine: 95
C for 8 min to activate the Taq; 94
C for 40 s;
C for 40 s (annealing); 72
C for 90 s (cycle twice, then
decrease anneal temperature by 1
C, repeat until cycled
at 52
C); 93
C for 40 s; 51
C for 40 s; 72
C for 90 s (repeat for
20 cycles). An aliquot of the product was run out on an
agarose gel to determine efficiency of amplification. Products
from different loci were diluted and mixed, depending on
the result from the agarose gel. One ml from each mix was
loaded onto an ABI 373 sequencer with 66 wells, set up for
GENESCAN, and run for 3–4 h. Alleles were sized against an
internal size standard. Genotype data were generated using
Data analysis
The following assumptions were made in organizing the
data for analysis:
1. Individuals with identical-sized alleles at all seven loci
have identical genotypes and belong to a single clone.
2. Genotypes found only once (termed here unique geno-
types) are most likely to be new recombinants from eggs on
peach produced by the previous autumn’s bisexual genera-
tion. These clones are considered in a subsequent paper.
3. Genotypes found on more than one sampling date and/or
in more than one location, termed here common genotypes,
are either definitely (if collected in more than one year or
at widely distant locations) or probably (if found on more
than one crop or at more than one location or time) ‘old’
clones that have overwintered parthenogenetically, so that
they do not form a regular part of an interbreeding
population and should not be included in the data set for
population genetics analysis (Sunnucks et al., 1997). The
incidence and distribution of these common clones was
investigated separately and is the subject of the present
4. A third category consists of genotypes found only at one
location and on one sampling date but represented by more
than one clonal lineage in the data set. This situation could
arise by: (i) multiple colonizations of the crop by winged
individuals of the same genotype; (ii) secondary spread by
individuals of the same genotype within the crop after a
single colonization; or (iii) as an effect of insufficient or poor
sampling. In such cases, it is not clear whether the genotype
should be treated as a new recombinant, or as an ‘old clone’,
so both possibilities were examined in the analysis.
Numbers of common genotypes were compared between
host plants and between regions using Chi-squared or using
Fisher’s exact test for small samples (< 10).
Frequency, distribution and properties of common genotypes
There were a total of 16 common genotypes, comprising
about half (49.0%) of the total samples in the data set
(table 2). The most frequently collected of these (no. 163) was
over three times more common than any other genotype
and made up 19.7% of the total data set. The colour, karyo-
type, GOT-1 genotypes and microsatellite allele sizes at
Table 2. Distribution of the 16 ‘common’ microsatellite genotypes of Myzus persicae among host plants.
Genotype no. Total no.
Crops Peach Tobacco Seedbeds Weeds All samples
No. % No. % No. % No. % No. %%
007 13 2 1.8 0 0 0 11 21.6 2.7
041 30 3 2.7 1 1.4 14 7.3 6 11.1 6 11.8 6.2
042 3 0 0 2 1.0 1 1.9 0 0.6
076 2 0 0 2 1.0 0 0 0.4
095 2 0 0 0 2 3.7 0 0.4
097 5 0 0 0 1 1.9 4 7.8 1.0
099 20 3 2.7 0 4 2.1 6 11.1 7 13.7 4.1
119 4 0 0 4 2.1 0 0 0.8
135 7 2 1.8 0 1 0.5 4 7.4 0 1.5
150 6 1 0.9 0 1 0.5 4 7.4 0 1.2
163 96 17 15.3 0 1.4 47 24.5 16 29.6 15 29.4 19.7
164 19 2 1.8 0 16 8.3 0 1 2.0 3.9
172 20 8 7.2 0 5 2.6 6 11.1 1 2.0 4.1
176 4 4 3.6 0 0 0 0 0.8
184 2 2 1.8 0 0 0 0 0.4
189 3 1 0.9 0 2 1.0 0 0 0.6
on each host 45 2 98 46 45 236
on each host 111 74 192 54 51 482
% common on each host 40.5 2.7 51.0 85.2 88.2 49.0
Chi-squared 1.5
Total no. of samples (second column) = number of separate samples collected of that clone. Proportion (%) on crops, peach, etc. is the
proportion of total samples from each host that were that clone. Field crops other than tobacco (cabbage, pepper, potato, etc.) are pooled
as ‘crops’. Proportion (%) of all samples (final column) = proportion of all 482 samples that were that clone. N
on each host = total
number of samples from that host that were common genotypes. N
on each host = total number of samples from that host.
Chi-squared is calculated on the basis of the number of samples of common genotypes expected, if each host had the same proportion
(0.490) of common genotypes as the total data set (
P < 0.0001). Proportion ( %) of common on each host = proportion of total number of
samples from that host that were common genotypes.
Population structure of Myzus persicae
Page 5
seven loci for genotype 163 and the next five most
frequently-collected genotypes (i.e. all those collected more
than ten times, and together comprising 40.7% of all samples
collected) are given in table 3.
Considered together, the frequency of collection of the 16
common genotypes in populations on field crops, both of
tobacco and other crops, did not depart significantly from
that expected on the basis of their representation in the total
data set. Common genotypes were not collected on peach,
except for single collections of each of the two commonest
genotypes (041 and 163). They did, however, account for
most of the samples taken from tobacco in seedbeds and
almost all of the samples collected from overwintering
populations on weeds (table 2).
Looking separately at the occurrence of the six common-
est genotypes (fig. 2), five of them were collected from both
tobacco and non-tobacco crops. Genotype 007 was found on
weeds in two successive winters and on pepper in a single
region in one year but was never collected on tobacco.
However, the numbers were too small for this to be
significant. Some of the other ten common genotypes
were sampled only either from tobacco crop and seedbeds
(e.g. genotypes 042, 076, 095, 97, 119) or from other crops
(e.g. genotypes 176, 184), but the numbers were too low for a
reliable conclusion.
When Greek regional differences were examined, the
frequency of occurrence of common genotypes was found
to be highly correlated with the relative abundance of the
primary host (fig. 1). In northern mainland Greece, the
majority of clones analysed from summer field crops had
unique genotypes. Around the sampling sites in this region,
the cultivated land devoted to peach constitutes about 95%
of the total peach-growing area in Greece. Some commercial
peach orchards also occur in the east-central coastal region,
near Volos (Anon., 1995), and here samples from pepper also
had a majority of unique genotypes. In the other regions of
mainland Greece, peach is not cultivated or only scattered
small orchards are present. In the central region, c. 150 km
further south of the main peach-growing area and c . 100 km
west of Volos, the proportions were reversed, with common
genotypes predominating in the tobacco-growing region
around Karditsa. Further south still, unique genotypes were
rarely collected.
In southern Italy, samples were mostly from tobacco and
had a high proportion of common genotypes, like those in
central and southern mainland Greece. Here there was,
however, no correlation with the presence of the primary
host, as peach orchards were common in the tobacco-
growing areas, as in northern Greece. The contrast between
these two regions has already been reported and discussed
(Margaritopoulos et al., 2003).
Five of the six commonest genotypes occurred in the
north, central and south of mainland Greece, and three of
these were also the predominant genotypes on tobacco in
southern Italy (fig. 3). However, none of the six commonest
Table 3. Colour, karyotype, glutamate oxaloacetate transaminase-1 genotype (GOT-1) and microsatellite allele sizes at seven loci for the
six most frequently collected clones of Myzus persicae.
Proportion of
all samples
Colour Karyotype GOT-1 Microsatellite loci
myz 2 myz 3 myz 9 myz 25 M35 M37 M40
007 0.027 Green Normal ff 177 177 121 121 196 196 118 122 181 197 155 155 132 138
041 0.062 Red Translocated ss 177 193 109 119 210 226 120 120 185 189 153 161 138 138
099 0.041 Red Normal ff 189 189 109 119 208 218 120 124 185 199 155 163 138 138
163 0.197 Red Translocated ss 179 191 125 125 206 214 120 120 201 201 153 155 138 138
164 0.039 Red Translocated sf 193 199 109 119 224 228 120 120 185 185 153 161 138 140
172 0.041 Green Normal sf 189 189 119 119 218 218 120 120 181 185 161 161 138 138
‘Normal’ means of normal 2n = 12 karyotype; ‘translocated’ means 2n = 12 with autosomal 1,3 translocation; ff ’, ss and sf are,
respectively, homozygous fast, homozygous slow and heterozygous forms of GOT-1.
007 041 099 163 164 172
selpmas fo )%( noitroporP
Fig. 2. Distribution of samples of the six commonest genotypes
of Myzus persicae on herbaceous hosts in mainland Greece and
southern Italy, compared with distribution of all samples. (For
further explanation of host plants see table 3.) (
, tobacco;
, other crops; , seedbeds; , weeds.)
North Central Central-
South South Italy
selpmas fo rebmuN
Fig. 3. Occurrence of the six commonest genotypes of Myzus
persicae according to region. (
, 007; , 041; , 099; , 163; , 164;
K, 172.)
R.L. Blackman et al.
Page 6
genotypes was found on pepper and tobacco at Xanthi in
north-east Greece, and on pepper in the east-central region
near Volos. Genotype 007, which was found overwintering
on weeds but not collected from tobacco, was only collected
in the northern region.
Numbers of alleles per locus tended to be higher in the
more northerly populations, but southern populations, con-
sisting almost entirely of common genotypes, were, never-
theless quite polymorphic (fig. 4) because of the low number
of alleles they shared.
Correlation of common genotypes with life cycle traits
Life cycle categories of eight of the common genotypes
were tested as part of a more extensive study of life cycle
variation in Greek populations (Margaritopoulos et al., 2002,
2003). Almost all of them were classified as anholocyclic
(table 4). The holocyclic response of two lineages (out of
16 tested) of genotype 172 was perhaps due to contamination
or mislabelling of cultures.
The percentages of clonal lineages that were common
genotypes in each region were compared with the percen-
tages of anholocyclic lineages obtained from summer crops
in the same localities during May–August of 1998–1999 in a
more extensive study of life cycle variation in Greece and
southern Italy (Margaritopoulos et al., 2002, 2003). A few
lineages that were tested only in the present study were also
included. Correlation across all six regions was not signifi-
cant (Pearson’s correlation 0.73, n =6, P < 0.097), but only
because the north-east region was markedly deficient in
common genotypes, having only three of those found in
other regions, although it did have a high percentage of
anholocyclic lineages (fig. 1). The north-east differed from
the other regions in that only one crop of tobacco and one of
pepper were sampled, five days apart. Most of the genotypes
in each of these populations were collected more than once,
but were outside our definition of common genotypes,
because they were found at only one time at one location.
Also, in central-eastern Greece, no common genotypes were
found, but some genotypes were collected more than once in
this locality. When these clonal lineages, plus other geno-
types represented more than once in other populations, were
added to the numbers of lineages of common clones, there
was a very close correlation (Pearson’s correlation 0.891,
n =6, P < 0.02) with the percentages of anholocyclic lineages
across all regions (fig. 1). Photoperiodic responses of 13
of the 17 genotypes multiply represented within populations
were tested and they were found to exhibit both anholocyclic
and holocyclic traits (table 4). Four out of the five north-
eastern genotypes were anholocyclic.
The incidence and distribution of the common genotypes
revealed by microsatellite genotyping can be related to
previous findings of patterns of variation in M. persicae
populations in mainland Greece (Margaritopoulos et al.,
2000, 2002; Zitoudi et al., 2001). About half of all samples
were common genotypes, and these dominated populations
on field crops, especially tobacco, in central and southern
Greece. Four of the five commonest genotypes on tobacco
were red in colour and account for the predominance of red
clones in central and southern tobacco-growing regions.
In laboratory tests, common genotypes were found to be
predominantly anholocyclic, and this explains their preva-
lence in populations overwintering on weeds, as well as in
tobacco seedbeds, which are colonized early in spring, before
the main migration from peach (Tsitsipis et al., 2004). The
very marked north–south gradient in the proportion of
Myz 2 Myz 3 Myz 9 Myz 25 Mp 35 Mp 37 Mp 40
selella fo rebmuN
Fig. 4. The number of alleles at each locus of Myzus persicae in
each region on summer secondary hosts. (
, north; , central; &,
, south Italy.)
Table 4. Life cycle categories of genotypes of Myzus persicae
multiply represented in the data set, as indicated by their
responses to a short photoperiod regime in laboratory tests.
Genotype no. No. of
Anholocyclic Holocyclic
Common genotypes
007 1 1 0
041 17 17 0
099 9 9 0
135 3 3 0
150 5 5 0
163 52 52 0
164 4 4 0
172 16 14 2
Genotypes represented multiply in single populations
017 (NE, pepper) 3 0 3
106 (NE, pepper) 2 2 0
176 (NE, pepper) 2 2 0
043 (NE, tobacco) 4 4 0
119 (NE, tobacco 4 4 0
024 (N, pepper) 2 0 2
062 (N, tobacco) 2 0 2
065 (N, tobacco) 2 0 2
216 (N, cabbage) 2 2 0
092 (EC, pepper) 1 0 1
040 (C, tobacco) 2 2 0
095 (C, seedbed) 2 2 0
168 (C, tobacco) 2 2 0
Holocyclic = lineages responding to short day by producing
exclusively males and matting females; anholocyclic = function-
ally parthenogenetic, this category includes all lineages continu-
ing to reproduce parthenogenetically in short days including
those able to produce a few males and/or mating females.
Population structure of Myzus persicae
Page 7
common genotypes (fig. 1) might seem to be explicable
simply in terms of the availability of the primary host. Away
from the commercial peach-growing region in the north, few
primary hosts are available, so that the predominant geno-
types will be those that overwinter parthenogenetically.
Peaches are grown in the region of Volos, in eastern central
Greece, which explains why the proportion of common
genotypes is much lower there than about 100 km inland,
in the tobacco-growing region near Karditsa, where there
are no peaches. The relative incidence of holocycly
and anholocycly in aphids can often be related to the
prevailing winter temperature, e.g. in S. avenae (Simon et al.,
1999; Dedryver et al., 2001), Macrosiphum rosae (Linnaeus)
hrmann & Tomiuk, 1988), Acyrthosiphon pisum (Harris)
(MacKay et al ., 1993) as well as M. persicae (Blackman, 1974;
Guillemaud et al., 2003; Vorburger et al., 2003), but this does
not seem to apply at the local level in Greece. For example,
winter temperatures at Karditsa, in central Greece, and
Katerini-Meliki, in the north, were similar. Also, further
north around Xanthi, most of the genotypes overwintered
parthenogenetically (see also Margaritopoulos et al., 2002).
Anholocyclic genotypes of M. persicae can also survive
more severe winters, e.g. much further north in western
Germany, where all clonal lineages from tobacco were found
to overwinter parthenogenetically (Kephalogianni et al.,
2002). The situation in mainland Greece somewhat resembles
that in Victoria, Australia, where the regional availability of
peach limits the success of holocyclic genotypes, although
winter temperature affects the geographical distribution of
anholocyclic clones (Vorburger et al., 2003).
A more detailed examination of the results indicates that
other factors are also involved. In the north-east, at Xanthi,
there is no commercial peach-growing, yet only three of the
16 common genotypes and none of the six commonest were
found. Most of the Xanthi genotypes were collected more
than once in the two sampled populations, and all except
one of the clones tested for life cycle category were func-
tionally anholocyclic (i.e. overwinter parthenogenetically),
but fell outside our working definition of common geno-
types, because they were neither collected at more than one
site nor on more than one occasion. In fact, the populations
that were sampled at Xanthi, both on pepper and tobacco,
proved to be very distinct genetically from those collected
elsewhere (Margaritopoulos et al., 2007). Evidently these
north-eastern populations are somewhat isolated.
The question that arises is why common genotypes,
which seem to be somehow tolerant to the winters usually
encountered in Greece, do not predominate in the peach-
growing regions in the north. The cold resistant diapause
egg provides higher opportunities for survival during the
winter but the crucial factor may be the rapid increase of
aphid populations on peach during spring growth, where
spring migrants leaving peach in huge numbers relative to
winged females arising from populations that have over-
wintered parthenogenetically on winter hosts. Other forms
of interclonal selection may also exist in the examined
populations. Genotypes identified by either their DNA (this
study) or by their photoperiodic response (Margaritopoulos
et al ., 2002) as having had a sexual phase on peach can rarely
be found in localities 100–150 km away from peach-growing
regions. Aphids are able to migrate over long distances, e.g.
R. padi (Delmotte et al., 2002), S. avenae (Llewellyn et al., 2003),
the commonest genotypes in this study; but the success
rate of migration may be low (Loxdale et al., 1993; Loxdale
& Lushai, 1999). Thus, local selection for specific genotypes
may be responsible for the low frequencies of unique geno-
types in areas away from the peach-growing regions.
The hypothesis that common genotypes prevail solely
because of the absence of peaches breaks down completely
in southern Italy, where in the region of Caserta there are
plenty of peach orchards, often in close proximity to tobacco
fields, as in northern Greece. Yet populations sampled on
tobacco consist almost exclusively of three common geno-
types, and 95% of the clonal lineages examined for life cycle
category were functionally anholocyclic. In addition, multi-
variate morphometric analysis separated the aphids origi-
nating from peach in Caserta from those collected on tobacco
(Margaritopoulos et al., 2003). It seems that populations on
peaches in southern Italy, unlike those in northern Greece,
lack the genetic capability to colonize tobacco. Three of the
five commonest genotypes sampled on tobacco in Greece
predominated also on tobacco in southern Italy. The
commercial production of tobacco in both Greece and Italy
is a recent event. We do not know, however, whether these
genotypes invaded and dispersed after the establishment of
the crop or were created later. Nevertheless, it appears that
some genotypes of the tobacco-feeding populations have the
ability to succeed in various environmental conditions. Data
obtained by high resolution DNA analysis during the last
decade have shown that this phenomenon is quite common
among aphid species (Sunnucks et al., 1996; Fenton et al.,
1998; Wilson et al., 1999; Haack et al., 2000; Llewellyn et al.,
2003; Vorburger et al., 2003; Fuentes-Contreras et al., 2004).
The relative advantages of these three widespread clones
remain to be determined. Insecticide selection pressure is
one probable reason (Zamoum et al., 2005), but these clones
may have ‘general-purpose genotypes’ (Lynch, 1984) with
broad ecological tolerance and, thus, predominate through
interclonal selection in fluctuating environments.
The commonest genotypes (with the exception of 007)
identified in this study are clearly very successful colonizers
of field tobacco but are also capable of feeding on other
crops. Populations on tobacco can be very large, with dense
colonies forming particularly on upper parts of stems and
young leaves. In contrast, populations on other field crops,
even in the vicinity of heavily infested tobacco crops, are
very dispersed; and often the aphids can be found only after
searching many plants, and then only singly or in small
groups on the older leaves. These extreme differences in
population levels between tobacco and other crops are an
important consideration when looking at genetic variation
between crops. Genotypes that can colonize tobacco will
tend to be the dominant clones wherever tobacco is grown
and are also the clones most likely to be encountered on
other crops within tobacco-growing regions. No strong
evidence for host association among the common genotypes
was noticed, except in the case of one of the six commonest
genotypes (007), which was sampled from weeds and crops
but never from tobacco, and classified as a non-tobacco
feeding clone according to GOT-1 phenotype (homozygous
for fast form, ff; Blackman & Spence, 1992). However, none
of the genotypes sampled on pepper in eastern-central
Greece, where tobacco is not cultivated, was found in any
of the tobacco-growing regions. Previous morphometric
studies have discriminated populations from peach and
pepper in eastern-central Greece from those collected
from tobacco-growing regions either from tobacco or from
peach (Margaritopoulos et al., 2000, 2003). Performance
R.L. Blackman et al.
Page 8
and host-choice experiments (Nikolakakis et al., 2003;
Margaritopoulos et al., 2005) proved also that tobacco is less
preferable and suitable host compared to pepper for the
eastern-central populations, while the opposite was
observed for those from tobacco-growing regions.
In conclusion, we have shown that common (anholo-
cyclic) genotypes make up a large proportion of populations,
except where peaches are grown commercially, and that
the climatic selection of sex hypothesis (Blackman, 1974)
and its theoretical developments (Rispe et al., 1998), which
holds for various aphid species, does not seem to apply
at the local level in Greece. In southern Italy, common
genotypes predominate on tobacco even in a peach-growing
region, because the nearby populations on peach do not
have the genetic capability to colonize tobacco. Thus, local
factors may determine whether the holocyclic or anholo-
cyclic mode of reproduction predominates in any one
population. Several of the common clones occur in both
Greece and southern Italy and probably in other parts of
the Mediterranean area, if not further afield. Such informa-
tion is necessary for population genetic studies and in order
to study the dispersal of genotypes with economically
important traits such as host adaptation and insecticide
The distinction between the two strategies of overwinter-
ing, and their consequences with regard to population
structure on crops, is clear enough in the short term, but
it needs to be borne in mind that the common genotypes
are probably all capable of producing males and thus
contributing to the sexual phase. This will eventually result
in new recombinants that inherit the ability to overwinter
parthenogenetically (Blackman, 1972; Margaritopoulos et al.,
2002). This parallels the situation found in French popu-
lations of R. padi (Delmotte et al., 2001, 2002), where there is
similar life cycle variability, and similar multiple origins of
The authors thank D. Butos, K. Zarpas and S. Goudou-
daki of the University of Thessaly, K. Seidos of the Tobacco
Institute of Greece and L. Sannino of Istituto Sperimentale
per il Tabacco, Scafati, Italy, for help with collecting the
samples for cloning and microsatellite analysis, and Alex
Wilson for valuable comments on an earlier draft of this
paper. This work was supported by the Commission of the
European Communities Tobacco Information and Research
Fund, project 96/T/18 ‘Management of the insect pests and
viruses of tobacco using ecologically compatible techno-
logies’. It does not necessarily reflect the views of the
Commission and in no way anticipates its future policy in
this area.
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Population structure of Myzus persicae
Page 11
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    • "Microsatellite analysis has also been widely used to investigate the genetic structure of the M. persicae population. Bayesian clustering and admixture analyses helped classify green peach aphid genotypes into three groups, corresponding to the common persicae, the bisexual nicotianae, and unisexual nicotianae (Blackman et al., 2007). Angela (2006) classified 18 geographic populations of green peach aphids in Italy into two categories, and the genetic distance between these populations was positively correlated to the geographic distance. "
    [Show abstract] [Hide abstract] ABSTRACT: The tobacco aphid, Myzus persicae nicotianae (Hemiptera: Aphididae), is an important agricultural pest that feeds on host plants and transmits plant viruses in China. To effectively control this pest, we investigated the genetic variation and genetic structure of 54 populations of tobacco aphids collected in China, using five microsatellite loci. An average of 7 alleles with effective number ranging from 1.5 to 6.6 was detected using these five loci, and the average polymorphic information content (PIC) was 0.652, suggesting that the five selected microsatellite loci were polymorphic and suitable for the study of population genetics. The expected heterozygosities in the populations studied ranged from 0.128 and 0.653, with an average value of 0.464. However, the observed heterozygosities ranged from 0.250 and 0.942 (average = 0.735), revealing a high genetic variability and heterozygosity excess in the Chinese tobacco aphid populations. The global fixation index (FST) and mean gene flow (Nm) were 0.34 (P < 0.0001) and 0.50, respectively, suggesting the high genetic differentiation among Chinese populations. The 54 populations of tobacco aphids were classified into two groups. The populations did not cluster geographically, as populations from the same provinces were usually present in different clusters. This was also confirmed by the Mantel test, which showed no significant correlation between the genetic distance and geographical distance or altitude. Long distance migration might be responsible for the lack of distance-related isolation.
    Preview · Article · Dec 2015 · Genetics and molecular research: GMR
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    • "Molecular and morphological studies have revealed that populations of M. persicae on Nicotiana tabacum L. (Solanaceae) are genetically and morphologically different from those on other host plants, and support the existence of a host race associated with tobacco (Blackman, 1987; Blackman & Spence, 1992; Margaritopoulos et al., 1998 Margaritopoulos et al., , 2000 Margaritopoulos et al., , 2003 Margaritopoulos et al., , 2007a Margaritopoulos et al., , 2007b Zitoudi et al., 2001; Blackman et al., 2007). Microsatellite or DNA short tandem repeats (STR) are codominant markers that have been successfully used to provide information about the population structure in aphids in relation to their life cycle, host, geographical distribution and dynamics (Sunnucks et al., 1997; Simon et al., 1999; Delmotte et al., 2002; Guillemaud et al., 2003; Vorburger et al., 2003a; Vorburger, 2006; Blackman et al., 2007; Margaritopoulos et al., 2007a). In agricultural areas of south-eastern Spain, agroecosystems are very diverse, with a great variety of crops intermingling with uncultivated land harbouring many wild plant species that are potential hosts for M. persicae (Sanchez et al., 2011). "
    [Show abstract] [Hide abstract] ABSTRACT: Diverse agroecosystems offer phytophagous insects a wide choice of host plants. Myzus persicae is a polyphagous aphid common in moderate climates. During its life cycle it alternates between primary and secondary hosts. A spatial genetic population structure may arise due to environmental factors and reproduction modes. The aim of this work was to determine the spatial and temporal genetic population structure of M. persicae in relation to host plants and climatic conditions. For this, 923 individuals of M. persicae collected from six plant families between 2005 and 2008 in south-eastern Spain were genotyped for eight microsatellite loci. The population structure was inferred by neighbour-joining, analysis of molecular variance (AMOVA) and Bayesian analyses. Moderate polymorphism was observed for the eight loci in almost all the samples. No differences in the number of alleles were observed between primary and secondary hosts or between geographical areas. The proportion of unique genotypes found in the primary host was similar in the north (0.961 ± 0.036) and the south (0.987 ± 0.013), while in the secondary host it was higher in the north (0.801 ± 0.159) than in the south (0.318 ± 0.063). Heterozygosity excess and linkage disequilibrium suggest a high representation of obligate parthenogens in areas with warmer climate and in the secondary hosts. The F ST-values pointed to no genetic differentiation of M. persicae on the different plant families. F ST-values, AMOVA and Bayesian model-based cluster analyses pointed to a significant population structure that was related to primary and secondary hosts. Differences between primary and secondary hosts could be due to the overrepresentation of parthenogens on herbaceous plants.
    Full-text · Article · Mar 2013 · Bulletin of entomological research
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    • "Each aphid colony was genotyped using six previously described microsatellite loci (M2, M3, M25, M35, M37, M40 ) (Sloane et al., 2001; Wilson et al., 2002; Vorburger et al., 2003, Fuentes-Contreras et al., 2004 Malloch et al., 2006; Vorburger, 2005 Vorburger, , 2006 Blackman et al., 2007; Margaritopoulos et al., 2007a; Kasprowicz et al., 2008 ). Multilocus genotypes (MLG) were obtained after combining alleles from each amplified locus in the whole sample, which resulted in fifty different MLG (information regarding microsatellite profiles for each genotype and the number of copies for each MLG is provided in the Supporting information,Table S2). "
    [Show abstract] [Hide abstract] ABSTRACT: The development of insecticide resistance in pest insects is an increasing problem for agriculture, forestry and public health. Aphids are ubiquitous herbivorous insects, with approximately 4700 known species, of which less than 5% exploit the agricultural environment successfully. Of these, the peach-potato aphid Myzus persicae Sulzer is recognized as one of the most important pests worldwide because it has acquired resistance to many insecticides. Although resistance to insecticides provides important benefits for pests in agricultural fields that are treated with insecticides, it may be associated with fitness (or other) costs in environments that are insecticide free. In the present study, the fitness and energy costs that might be experienced by M. persicae in an insecticide-free environment when carrying at least one insecticide resistance mutation (IRM), or by having an increased production of esterases, are evaluated. The study investigates whether genotypes that have an IRM also have enhanced esterase production, whether there is any metabolic cost associated with insecticide resistance, and whether there are any fitness costs associated with insecticide resistance and metabolic expenditure. The intrinsic rate of increase, standard metabolic rate (i.e. a measure of maintenance costs) and constitutive esterase activity are determined for 30 different multilocus genotypes carrying (or not carrying) at least one of the two most frequent insecticide resistance mutations (MACE and kdr/super-kdr) that occur in Chile. The results show that genotypes carrying at least one IRM have higher levels of total esterase activity than genotypes without an IRM, that there is no evidence of an energy cost associated with total esterase activity or IRM, and no evidence for a reproductive fitness cost associated with total esterase activity, IRM or metabolic rate. The results agree with previous studies showing linkage disequilibrium between insecticide resistance mechanisms, although they contrast with those of studies that report fitness costs associated with insecticide resistance in Myzus persicae.
    Full-text · Article · Sep 2011 · Physiological Entomology
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