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76
Original Article
D. A. S. SMITH
ET AL.
HALDANES RULE IN HYBRID QUEEN BUTTERFLIES
Biological Journal of the Linnean Society, 2002, 76, 535544. With 2 figures
A cross between queen butterflies of the Palaeotropical species Danaus chrysippus and the Neotropical D.gilippus
was achieved with difficulty in both directions. Only one progeny (N = 70) was reared comprising sterile males and
inviable females in a precisely 1:1 ratio. Both prezygotic and postzygotic barriers to gene flow are strong. The result
supports Haldanes Rule, to which we propose a minor amendment. The F1 hybrids were intermediate for background
colour between the brown (genotype BB) of gilippus and orange (genotype bb) of chrysippus. Most F1 pattern characters were also intermediate. In polymorphic chrysippus populations, because Bb heterozygotes are brown, or
nearly so, we suggest the B allele may have evolved towards dominance in sympatry. Hybrid males show positive
heterosis for body size. The close similarity of male genitalia between the allopatric, genetically distant species
chrysippus and gilippus, compared to their divergence between gilippus and its largely sympatric sister species eresimus, suggest that reinforcement of sexual isolation or reproductive character displacement have evolved in
sympatry. 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 76, 535544.
INTRODUCTION
The queen butterflies Danaus (Anosia) chrysippus in
the Old World and D. (A) gilippus in the Americas have
both enjoyed a high profile in butterfly studies; and yet
their taxonomic status remains unresolved. In particular, Ackery & Vane-Wright (1984) say, we have been
unable to discover any apomorphies which characterize [gilippus] to the exclusion of D.chrysippus. They go
on to speculate, although the Old World chrysippus
can be defined by pattern characters . . . , it is so simi-
lar in all other known features to the New World gilippus that . . . the two may best be regarded as one
species. Our principal aim in attempting to hybridize
chrysippus and gilippus is to test the Ackery/VaneWright hypothesis, which would be supported if fertile
hybrids resulted from the cross.
The subgenus Anosia (queen butterflies) of the
genus Danaus (Order Lepidoptera, Family Nymphalidae, Subfamily Danainae, Tribe Danaini, Subtribe
Danaina) comprises four currently recognized species,
three from the New World and one from the Old World
(Ackery & Vane-Wright, 1984), as follows: D. (A) eresimus (Florida, Texas and Antilles south to the Amazon
Basin), D. (A) plexaure (central South America, south
of the Amazon, Bolivia and southern Brazil to Paraguay, Argentina and Uruguay), D. (A) gilippus (south-
2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 76, 535544
535
536
D. A. S. SMITH ET AL.
MATERIAL
MATING
ENCLOSURE
MORPHOLOGICAL
CONFIRMATION OF THE
BUTTERFLIES USED
2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 76, 535544
RESULTS
OBSERVATIONS
COPULATION
537
HYBRID
FITNESS
THE F1
HYBRID PHENOTYPE
2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 76, 535544
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D. A. S. SMITH ET AL.
Table1. Phenotypic characters scored for Danaus chrysippus dorippus, D.gilippus berenice and F1 hybrids
Character
1
2
3
4
5
6
7
8
9
D.chrysippus
D.gilippus
F1 hybrids
40.70.45 (N=14)
39.80.75 (N=12)
Tawny orange
Absent
39.60.43 (N=9)
36.81.40 (N=4)
Nutbrown
Present
Absent
Present
42.40.38 (N=16)
39.00.44 (N=13)
Intermediate*
93.1% penetrance
(N=29)*
Absent
Absent
Present
Absent
Single in 85.3%
(N=35)
Present
Double
Absent
Intermediate on d & v *
Narrowly black*
Narrow (2.5mm)
Pale
Notation: SE, standard error; fw, forewing; hw, hindwing; d, dorsal; v, ventral. *see text for more detail.
rich chocolate brown (Fig.1c,d). The hybrids are predominantly orange with more or less heavy brown
shading, on the dorsal side, in the basal areas of both
wings and extending along the costal margin of the
forewing to between one-third and two-thrids of its
length (Fig.1eh). Although the extent of brown is
variable, submarginal and marginal areas of both
wings (excepting the narrow black borders) are tawny
orange in all specimens.
4. The subapical, white spots in forewing spaces M2
and M3 of D.gilippus are homologous with the much
larger ones found in most D.chrysippus subspecies; the
spots are absent only from subspecies dorippus. This
character is penetrant in the F 1 hybrids, as small pale
spots on the forewing underside (93.1%, N =29) and, as
faint marks, on the upper side (69.0%, N =29). Expressivity of the character, when present, in the hybrids is
essentially uniform.
56. The 1113 conspicuous, extra, white spots, 3
in the postmedial area and 810 in the submarginal
area, on both forewing surfaces (spaces 2AR5) of gilippus, all of which are lacking in chrysippus ssp. dorippus, are also absent in the hybrids.
7. All gilippus have a pair of white spots (externae)
in forewing space R4, whereas in most chrysippus there
is a single, larger spot (Ackery & Vane-Wright, 1984).
In the chrysippus specimens we have examined
(N =35), 85.3% have a single spot that often clearly
results from fusion of two spots; the remainder, unlike
gilippus where the two spots are well separated, has a
2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 76, 535544
(a)
(b)
(c)
(d)
(e)
(f)
(g)
(h)
539
Figure1. (a) Danaus chrysippus dorippus male (ventral). (b) D.chrysippus dorippus female (dorsal). (c) D.gilippus berenice
male (ventral). (d) D. gilippus berenice female (dorsal). (e) F1 male (dorsal) from the cross chrysippus (male) gilippus (female).
(f) F1 female (dorsal). (g) F1 male (ventral). (h) F1 female (ventral). Scale bar=2cm.
2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 76, 535544
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D. A. S. SMITH ET AL.
Table2. Analysis of the number of spines on the aedeagi of male Anosia butterflies
Mean number of spines standard error
Species
Left (L)
Right (R)
Total
Ratio L/R
D. chrysippus dorippus
D. gilippus berenice
chrysippusgilippus F1
D. eresimus tethys
5.10.27
4.60.53
5.30.25
3.10.28
6.70.44
6.20.28
6.30.95
4.40.51
11.80.56
10.80.61
11.50.95
7.50.54*
0.720.05
0.750.09
0.890.11
0.840.14
23
13
4
10
DISCUSSION
THE F1
MALE
GENITALIA
HYBRID PHENOTYPE
2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 76, 535544
SEXUAL
ISOLATION
541
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D. A. S. SMITH ET AL.
HALDANES
EVIDENCE
REINFORCEMENT
OR REPRODUCTIVE CHARACTER
DISPLACEMENT
In a detailed comparison of evolutionary rates for preand postmating isolation, Coyne & Orr (1989) concluded that both evolved at a similar rate in Drosophila, although premating isolation appeared most
quickly between sympatric species (such as eresimus
and gilippus). On the other hand, in allopatric species,
such as gilippus and chrysippus, that probably speciated by dispersal across oceans and are now separated
by substantial genetic and geographical distances,
sexual isolation cannot result from selection. Hence,
while the potentially complete sexual isolation of gilippus and chrysippus is no surprise, it is probably a
pleiotropic consequence of independent genetic drift in
long-separated populations (Ritchie & Phillips, 1998)
rather than of selection. It is intriguing therefore
that the (eresimus + plexaure) aedeagus differs qualitatively (Fig.2) and quantitatively (Table2) from that of
(gilippus + chrysippus), whereas, among the latter pair
2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 76, 535544
ACKNOWLEDGEMENTS
All authors acknowledge assistance from Leverhulme
Trust Grant F/180/AP. DASS thanks Henry and Eliza
Harford for hospitality on Grand Cayman and assistance with food plants and transport. We are grateful
to George McGavin, Oxford University Museum of
Natural History, for the loan of specimens. Joanna
Liddiard drew Figure1.
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D. A. S. SMITH ET AL.
2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 76, 535544