Comparison of the Male Genitalia and Androconia of Pseudochazara Anthelea Acamanthis (Rebel, 1916) from Cyprus, Pseudochazara Authelea Anthelea (Hubner, 1824) from Mainland Turkey and Pseudochazara Anthelea Amalthea (Frivaldsky, 1845) from Mainland Greece

13 Pages·2002·5.9 MB·English

by  Andrew Wakeham-Dawson

1
Notalepid. 25 (4), published2003: 251-263 25
Comparison ofthe male genitalia and androconia of
Pseudochazara anthelea acamanthis (Rebel, 1916) from Cy-
prus, Pseudochazara anthelea anthelea (Hübner, 1824) from
mainland Turkey and Pseudochazara anthelea amalthea
(Frivaldsky, 1845) from mainland Greece (Nymphalidae,
Satyrinae)
Andrew Wakeham-Dawson1 Rob Parker2 Eddie John3 & Roger L. H.
, ,
Dennis4
1 The International Commission on Zoological Nomenclature, c/o The Natural History Museum,
Cromwell Road, London, SW7 5BD, Great Britain (e-mail: [email protected]); corresponding
author
2 66 Cornfield Road, Bury StEdmunds, Suffolk, IP33 3BN, GreatBritain
3 Davies Cottage, Penllyn, Cowbridge, Vale ofGlamorgan, CF71 7RQ, Great Britain
4 Department ofEntomology, The Manchester Museum, Manchester University, Oxford Road,
Manchester, Ml3 9PL, Great Britain
Summary. Statistical analysis ofmeasurements made on genitalia and androconia ofPseudochazara
anthelea acamanthis (Rebel, 1916) butterflies from Cyprus, P. anthelea anthelea (Hübner, 1924) from
mainlandTurkeyandP. antheleaamalthea(Frivaldsky, 1845) from mainlandGreeceshowsthatthereis
considerable overlap between the three taxa as represented by the specimens used in this study. The
general similarity ofthe genitalia and androconia ofthese specimens supports Olivier's (1996) syn-
onymy ofP. antheleaacamanthis with P. anthelea antheleabased on his study ofwing pattern.
Key words.Lepidoptera,Satyrinae,Pseudochazaraanthelea,genitalia,androconia,Cyprus,Greece,
Turkey, biometrics, statistical analysis.
Introduction
The genus Pseudochazara de Lesse, 1951 (type-species by original designation
Hipparchiapelopea Klug, 1832) consists ofover twenty species and subspecies that
are restricted to Europe andAsia. Gross (1978) reviewed the genus, but recent discov-
ery ofadditional species means that a fresh revision is now necessary and preliminary
work towards such a revision is underway (Wakeham-Dawson & Kudrna 2000;
Wakeham-Dawson& Dennis2001).AsnotedbyGross(1978), Hesselbarthetal. (1995)
and Wakeham-Dawson & Dennis (2001), Pseudochazara species can be divided into
two subgroups: (1) those that have male genitalia and androconia that are broadly
similar to the type species P. pelopea and (2) those that have male genitalia and
androconia that are broadly similar to P. anthelea anthelea (Hübner, 1824). It is in-
tended that these two groups be formally described as subgenera in the planned revi-
sion.
The P. anthelea anthe/ea-subgroup is represented in the area around the Aegean
Sea by a number of nominal subspecies. Olivier (1996) concluded, on the basis of
wing pattern examination, that the nominal subspecies Pseudochazara anthelea
©Notalepidopterologica, 16.06.2003.ISSN0342-7536
£~>^ Wakeham-Dawson, Parker,John&Dennis: MalegenitaliaandandroconiaofPseudochazara
acamanthis(Rebel, 1916)fromCyprusisconspecificwith/! antheleaanthelea(Hübner,
1824)frommainlandTurkey.However,hedidnotconsidermalegenitaliaorandroconia
in his deliberations. In continuation ofa long-running study ofthe butterflies ofCy-
prus (Parker 1983, John 2000) and as part ofthe revision ofthe genusPseudochazara
mentionedabove, measurements made onandroconiaandgenitaliafrom specimens of
P. anthelea acamanthis from Cyprus are compared in the current study with measure-
ments made on specimens ofP. anthelea anthelea from mainland Turkey. This paper
presents the results ofan analysis ofthese measurements and comments on the rela-
tionshipbetweenmainlandandCypruspopulations(subspecies). Italsocomparesthese
findings with androconia and genitalia measurements from specimens ofP. anthelea
amalthea(Frivaldsky, 1845)capturedinmainlandGreeceandareasjustnorthofGreece.
Methods
Sources of data and measurements .The genitalia and androconia
measurement data used in the current study are taken from 60 male Pseudochazara
butterfly specimens: 23 P. anthelea acamanthis, 20 P. anthelea anthelea and 11 P.
anthelea amalthea. The locations in which these specimens were captured are pro-
vided in theAppendix.
ThegenitaliahavebeenmeasuredusingthemethodsdescribedinWakeham-Dawson
&Dennis (2001) andthe androconiausingmethods describedinWakeham-Dawson&
Kudrna (2000) (also see Figs. 1-3), although in the current study androconia were
mounted under cover slips in DPX medium on microscope slides, rather than being
preserved dryunderthe cover slips (as inWakeham-Dawson & Kudrna2000). Diago-
Fig. 1. Diagram ofmale genitaliaofPseudochazaraanthelea subspecies, aa= apex angularis; b=bra-
chium; f= furca; p =penis; s= saccus; t=tegumen; u=uncus; v=valve; vi=vinculum. Terminology
afterHiggins (1975).
Notalepid. 25 (4), published2003: 251-263 253
Fig. 2. Diagram ofmeasurements made on male genitaliaofPseudochazaraanthelea subspecies. DL=
diagonal length,measuredfromdorsaljunction oftegumenanduncustobaseofsaccus(the linerunning
at the same angle as the vinculum); VL (indicated by the solid line running beneath the valve) = valve
length; VB =valvebreadth, measuredat0.5 mm fromvalveapex andat90° tothe lineVL; UL=uncus
length, measured from uncus apex to mid-point betweenjunction oftegumen and uncus; UB = uncus
breadth, measured at 0.5 mm from uncus apex and at 90° to the line UL; BL = brachium length, meas-
ured fromapex ofbrachiumtodorsaljunction oftegumen andbrachium; BB=brachiumbreadth, meas-
ured acrossjunction oftegumen and brachium; TL=tegumen length, measured from dorsaljunction of
tegumen and uncus to junction ofapex angularis and vinculum; TB = tegumen breadth; PL = penis
length; PB = maximum penis breadth.
nal length (DL) is divided by valve length (VL) to produce a unit-less ratio D, which
measures overall proportion (shape) of the genitalia independently of size variation
between individuals in ataxon. Similarly, valve length (VL) isdividedbyvalvebreadth
(VB) to produce a ratio V, representing valve shape. Uncus length (UL) is divided by
uncus breadth (UB) to produce a ratio U, representing uncus shape. Brachium length
(BL) is divided by brachium breadth (BB) to produce a ratio B, representing brachium
shape. Tegumen length (TL) is divided by tegumen breadth (TB) to give a ratio T,
representing tegumen shape, and penis length (PL) is divided by uncus breadth (UB)
(as penis breadth, PB, is not available forall specimens) to give a ratio PL In addition,
penis length (PL) is divided by penis breadth (PB) (with linear regression estimates of
PB for thirteen specimens; r = 0.67, F3 42 = 11.59, p < 0.00001) to give a ratio P2.
254 Wakeham-Dawson, Parker, John& Dennis: MalegenitaliaandandroconiaofPseudochazara
Fig. 3. Diagram ofPseudochazara anthelea androconium and the
measurements made. AL = androconium length, measured from ba-
sal stalk (bs) to terminal points (tp) at apex; AB = androconium
breadth, measured across widestpart ofandroconium. Terminology
after Kudrna (1977).
Androconium length (AL) is divided by androconium breadth (AB) to give ratio A.
This provides 21 variables (13 measurements and 8 ratios) for analysis.
Statistical analysis. All variables, with the exception of BB, are nor-
mally distributed. These variables are analysed untransformed. BB shows a positive
skew and is treated with a log transformation before analysis. Data are analysed
10
using one-way analysis ofvariance (ANOVA), stepwise discriminant function analy-
sis (DFA) and Euclidean non-metric multi-dimensional scaling (NMMS) (see Sneath
& Sokal 1973; Statsoft 1999). These methods have been shown to be effective in re-
vealing morphological relationships between taxa (e.g. Wakeham-Dawson & Dennis
2001).
Results
The means, standard errors and maximum and minimum values ofmeasurements
&
and ratios from genitalia (Fig. 2) and androconia (Figs. 3 4) ofall three taxa are
presented for comparison in Tables 1 (measurements) and 2 (ratios). Only five ofthe
13 measurements (VL, UL, log BB, TB, PL) reveal significant differences (p<0.05)
10
between the taxa, with PB marginally significant atp=0.06, whenANOVAis applied
(Table 3). For the eight ratios, only three (U, B and PI) show significant differences
whenANOVA is applied (Table 4).
Inthese cases, the taxonomicpattern is similarin all variables, except forthe com-
parison ofBB andratioB (brachium length, BL, dividedbybrachiumbreadth, BB).P.
anthelea acamanthis is distinct from P. anthelea anthelea (significant differences,
p<0.05, shown in all variables exceptB) andP. anthelea amalthea (significant differ-
Notalepid. 25 (4), published2003: 251-263 255
Fig 4. The androconia ofP. anthelca anthelea from mainland Turkey [specimen nos. 443 (diagram a),
345 (b, bi, bii), 444 (c), 192 (d, di)] and P. anthelca acamanthis from Cyprus [specimen nos. 437 (dia-
grame),439(f),438 (g),436(h),435 (i)]. Notethevariation in androconium baseshapebothwithin and
between specimens. The androconia ofP. anthelca amalthea (not illustrated) are similar in shape and
showsimilarvariation inbaseshapetothoseillustrated. There isnosignificantdifferenceintheshapeof
the androconia between any ofthese taxa (seeTables 3 & 4).
—
256 Wakeham-Dawson, Parker, John&Dennis: MalegenitaliaandandroconiaofPseudochazara
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Notalepid. 25 (4), published2003: 251-263 257
Tab. 2. Summary statistics (means, standard errors (SE) andminimum (Min) andmaximum (Max)) for
genital and androconial ratios in three taxa ofPseudochazara butterflies (no units). N = number of
specimens. See text for explanation.
Taxon Pseudochazaraantheleaacamanthis Pseudochazaraantheleaanthelea Pseudochazaraantheleaamalthea
Variable Mean Min Max SE Mean Min Max SE Mean Min Max SE
V 14.21 9.37 19.00 0.556 15.94 10.80 21.00 0.719 15.75 8.71 24.08 1.213
u 9.62 6.50 12.00 0.272 10.76 8.75 12.80 0.222 10.68 8.33 13.00 0.392
B 3.12 2.38 3.85 0.071 2.95 2.20 3.57 0.087 2.65 1.89 3.43 0.095
T 1.21 1.10 1.30 0.012 1.15 0.91 1.41 0.032 1.18 0.98 1.33 0.023
PI 18.40 14.38 25.60 0.503 20.06 16.92 22.50 0.395 20.35 16.67 26.30 0.657
P2 9.23 8.00 10.67 0.152 9.26 8.21 10.92 0.139 9.63 8.78 10.61 0.144
D 1.01 0.87 1.09 0.011 0.98 0.92 1.03 0.008 0.96 0.65 1.11 0.028
A 11.40 8.13 14.50 0.313 10.95 5.88 14.23 0.437 11.85 8.68 16.83 0.564
PseudochazaraantheleaacamanthisN=23,PseudochazaraantheleaantheleaN=20,PseudochazaraantheleaamaltheaN=17
Tab.3. One way analysis ofvariance(ANOVA) forgenital andandroconial measurements inthreetaxa
ofPseudochazara butterflies. Significant effects (p<0.05) printed in bold face.
OnewayANOVA
Variable SS effect df MS SSerror dferror MS error F P
effect effect
VL 0.5698 2 0.2849 2.0417 57 0.0358 7.95 0.0009
VB 0.0016 2 0.0008 0.1145 57 0.0020 0.41 0.67
UL 0.1418 2 0.0709 0.3695 56 0.0066 10.74 <0.0001
UB 0.0004 2 0.0002 0.0109 57 0.0002 0.95 0.39
BL 0.0116 2 0.0058 0.2089 57 0.0037 1.58 0.23
BB 0.0037 2 0.0019 0.0087 57 0.0002 12.25 <0.0001
DL 0.2039 2 0.1019 2.7122 57 0.0476 2.14 0.13
TL 0.0506 2 0.0253 1.2594 57 0.022 1.15 0.33
TB 0.0815 2 0.0408 0.4603 56 0.0082 4.96 0.0104
PL 0.4427 2 0.2213 0.9436 56 0.0168 13.14 <0.0001
PB 0.0019 2 0.0010 0.0136 44 0.0003 3.11 0.06
AL 0.0003 2 0.0001 0.0080 54 0.0001 0.88 0.44
AB 0.0000 2 0.0000 0.0006 54 ().()()()() 0.98 0.38
ences shown in all variables), but P. anthelea anthelea and P. anthelea amalthea are
homogeneous (only log, BB and B show a significant difference).
()
In stepwise discriminant function analysis (DFA), only three of the variables {PI,
log BB and UL) are retainedthatprovide significantdiscrimination between taxawhen
10
all three groups (P. antheleaacamanthis, P. antheleaanthelea and P. antheleaamalthea)
are compared orwhen only two groups (P. antheleaacamanthis vs. P. antheleaanthelea
258 Wakeham-Dawson, Parker, John&Dennis MalegenitaliaandandroconiaofPseudochazara
Tab. 4. One way analysis ofvariance (ANOVA) for genital and androconial ratios in three taxa of
Pseudochazara butterflies. Significant effects (p<0.05) printed in bold face.
Variable SSeffect dfeffect MSeffect SSerror dferror MSerror F P
V 38.24 2 19.12 753.02 57 13.21 .1.447 0.244
U 17.40 2 8.70 97.84 57 1.72 5.068 0.009
B 2.16 2 1.08 7.94 57 0.14 7.760 0.001
T 0.03 2 0.02 0.60 57 0.01 1.626 0.206
PI 46.34 2 23.17 304.66 57 5.34 4.335 0.018
P2 1.74 2 0.87 24.67 57 0.43 2.015 0.143
D 0.02 2 0.01 0.29 57 0.01 2.369 0.103
A 7.56 2 3.78 208.69 57 3.66 1.032 0.363
and P. anthelea amalthea amalgamated) are compared. DFA ofthe three groups gives
70% (18 individuals misclassified) correct classification (Wilks'À,= 0.42, F = 9.92,
A (6?110)
pO.0001). plot ofthe firsttwo roots shows thatP. anthelea anthelea andP. anthelea
amalthea almost completely overlap. However, P. anthelea acamanthis would fall
outside these two groups ifit were not for five ofthe P. anthelea anthelea specimens
and the position of one P. anthelea acamanthis specimen (Fig. 5). DFA ofthe two
groups gives 90% (6 individuals misclassified) correct classification (Wilks'A,=0.50,
F =18.95, pO.0001). This shows good separation, but not enoughto avoid confu-
(3 56)
sion in a blind trial.
Two Euclidean non-metric multidimensional scaling (NMMS) plots based on all
variables andjust on ratios are virtually identical and show that there is considerable
overlap between the P. anthelea acamanthis, P. anthelea anthelea and P. anthelea
amalthea specimens (Fig. 6 for all variables).
Discussion
Comparison of genitalia and androconia morphology
between populations. AnalysisofvarianceshowsthatP. antheleaacamanthis
specimens differ significantly from the two mainland taxa specimens (P. anthelea
anthelea and P anthelea amalthea) in a number ofvariables. Similarly, P. anthelea
acamanthis specimens are largely distinct from P anthelea anthelea and P anthelea
amalthea in DFAaxes. However, Euclideanplots show considerable overlap between
the three taxa as representedby the specimens used in this study. The general similar-
ity ofthe genitalia and androconia ofthese specimens supports Olivier's (1996) syn-
onymyofP. antheleaacamanthis withP. antheleaantheleabasedonhis studyofwing
pattern. Perhapsmoresurprisingistheapparentsimilaritybetweeni? antheleaanthelea
and P anthelea amalthea. However, the similarity between these two taxa has been
notedpreviouslyby Wakeham-Dawson & Dennis (2001), and although these taxa are
treated as distinct species by many authors (e.g. Kudrna 2002), they may in fact be
conspecific (i.e. capable ofinterbreedingto produce fertile offspring). The differences
Nota lepid. 25 (4), published2003: 251-263 259
3.0-
2.5 -
2.0 -
1.5 - +
1.0 - + +
+
0.5 -
CM
I 0.0- D + + +
+ +
-0.5 -
+
*
-1.0 - a ++
D
-1.5 - D + D +
-2.0 - a + P. acamanthis
P. anthelea
-2.5 -
% -3 -2 -1 1 2 3 A P. amalthea
Root 1
Fig. 5. PlotofthreePseudochazaraantheleataxainthefirsttworoots(Root 1 vs. Root2)ofadiscrimi-
nant function analysis (DFA).
.... ....
2.0 i i i
1.5
1.0
•
0.5
CM V
cn 0.0 <?
-0.5
1.0
1.5
AlienationK=0.11
KruskalstressS= + P acamanthis
-2.0 P. anthelea
1.5 -1.0 -0.5 0.0 0.5 10 15 20 25 a P. amalthea
Axis 1
Fig.6.Non-metrictwo-dimensional plot(Axis 1 vs.Axis2)ofthreePseudochazaraantheleataxabased
on Euclidean distances for all genitalia and androconia variables.
^°U Wakeham-Dawson, Parker, John&Dennis: MalegenitaliaandandroconiaofPseudochazara
between P. anthelea acamanthis and P. anthelea anthelea and P. anthelea amalthea,
and the similarities between P anthelea anthelea and P. anthelea amalthea indicated
by the current small-scale study suggest that a larger study including more specimens
anduse ofmolecular datacouldprovide some revealing insights into the relationships
between these nominal taxa.
Gene flow between p opu1 ati on s . Geological evidence suggests that
formation ofthe island ofCyprus began between 230 and 95 million years ago as it
was forced up from the bed ofthe now Mediterranean Sea by movement oftectonic
plates. 'A land area of some sort has existed on the present site of the island from
MiddleMiocene (abouttenmillionyears ago)times onwards' (Greensmith 1998,p.6).
As aresult, the formation ofthe island almost certainlypre-dates the formation ofthe
taxa we know as subspecies ofP. anthelea. The population on Cyprus was probably
established by individuals immigrating from the mainland in the last million or so
years (althoughthe actual age ofthese taxacan onlybe guessed at). The most suitable
opportunities for migration would have been during the climate changes, lower sea
levels and extended shorelines associated with ice-sheet formation between the Last
GlacialMaximumandthe earlyHolocene (Zonnerveld 1995; Lambeck&Bard2000).
As Cyprus is only70kmfrommainlandTurkey, the islandpopulationhasprobably
been sporadically augmented inthe pastwith individuals from the mainland, andvice
versa. However,P. antheleaacamanthis isnowadaysthemost sedentaryofthe Cyprus
Satyrinae interms ofitsvertical distribution. Hipparchiacypriensis (Holik, 1949) (an-
other member of the Satyrinae present on Cyprus) has been observed engaging in
m &
seasonally reversed migration between sea level and 1900 (John Parker 2002).
However, P. anthelea acamanthis does not show this type of behaviour. It is most
m &
frequently encountered above 1000 (Makris in press; R. Parker E. John, unpub-
lished data) and although it does occur at intermediate elevations, only one specimen
m
(an individual nectaring on Lantana) has been recorded from as low as 250 (D.
Haines, unpublished data). It is therefore hard to envisage specimens ofthe present
day P. anthelea acamanthis dispersing in numbers from higher elevations. It is even
harder to contemplate the species embarking on a crossing to the mainland or vice
versa.
Thisviewis supportedbyananalysisofnearly300 sightingsofP. antheleaanthelea
recorded in Hesselbarth et al. (1995). On the Turkish mainland, only three specimens
m
(1% ofsightings) are listed as being noted below an altitude of250 while, in sharp
m
contrast, 282 (96%) were found above 500 (including 237 records (81%) observed
at 1000 morhigher). Changes inclimate oragriculturalpracticesmayhaveinfluenced
behaviour in recent centuries, confining the species to generally higher elevations.
Althoughthepopulation on Cyprus may havepreviouslybeen in reproductive contact
with mainland populations, it appears to be effectively isolated at present.
As there are only slight differences betweenthe genitalia and androconiamorphol-
ogyintheisland(P. antheleaacamanthis) andTurkishmainland(P. antheleaanthelea)
populations, itwouldappearthatgene flowprobablydidoccurinthepastbetweenthe
two populations. For similar reasons, it would also appear that there is or, until re-
cently, has been regular gene flow between mainland Greece (P anthelea amalthea)